NOAA Technical Memorandum NOS OR&R 8

 

Toxicity of Oil to Reef-Building Corals:

A Spill Response Perspective

Seattle, Washington

September 2001

noaa NATIONAL OCEANIC AND ATMOSPHERIC ADMINISTRATION

National Ocean Service
Office of Response and Restoration

National Ocean Service

National Oceanic and Atmospheric Administration

U.S. Department of Commerce

NOAA is responsible for protecting and restoring marine and coastal environments

impacted by spills and hazardous substance releases. The Office of Response and

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Guard in the coastal zone, or EPA in inland areas).

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negotiate protective remedies with the responsible parties to ensure that cleanup,

restoration, and recovery are appropriate and fully monitored.

While the HAZMAT and CPR divisions work to prevent and minimize injury to natural

resources during spill response and waste site remediation activities, the Damage

Assessment Center focuses on addressing the injury that remains after the cleanup or

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NOAA Technical Memorandum NOS OR&R 8

Toxicity of Oil to Reef-Building Corals:

A Spill Response Perspective

Gary Shigenaka

Hazardous Materials Response Division

Office of Response and Restoration

National Oceanic and Atmospheric Administration

7600 Sand Point Way N.E.

Seattle, Washington 98115

M

A

O

N

NAL OCE I A C AND AT OSPHERIC ADMINISTR T OI N

I TA NU.S. DEPA EN T T M R

OF COM MERCE

Seattle, Washington

Donald L. Evans, Secretary Scott B. Gudes Margaret A. Davidson

U.S.Department of Commerce Acting Under Secretary for Acting Assistant Administrator

Oceans and Atmosphere for Ocean Services and

and NOAA Administrator/ Coastal Zone Management
Deputy Under Secretary for NOAA National Ocean

Oceans and Atmosphere Service
Office of Response and Restoration

National Ocean Service

National Oceanic and Atmospheric Administration

U.S. Department of Commerce

Silver Spring, Maryland

NOTICE

This report has been reviewed by the National Ocean Service of the National Oceanic and

Atmospheric Administration (NOAA) and approved for publication. Such approval does not signify

that the contents of this report necessarily represent the official position of NOAA or of the

Government of the United States, nor does mention of trade names or commercial products

constitute endorsement or recommendation for their use.
ACKNOWLEDGMENTS

As this manuscript is largely a review of existing knowledge, the significant effort in

creating it was the process of identifying and retrieving relevant information. As such,

two people in particular were instrumental in helping me to accomplish the task:

NOAA Seattle Regional Library Director Maureen Woods; and NOAA/OR&R Librarian

John Kaperick. They endured seemingly never-ending requests for increasingly obscure

references.

Dr. Jacqueline Michel of Research Planning, Inc. reviewed the manuscript in typically

painstaking fashion and improved it greatly. She also provided photographs of the

TROPICS experiment. Dr. Cindy Hall of the Waikiki Aquarium also reviewed the

document and directed me to key references on coral reproduction. Dr. John Cubit of

NOAA shared some of his personal photographs from the Bahía Las Minas spill. Dr. Iva

Stejskal of Apache Energy Limited in Perth, Australia, Dr. William Gardiner, and Dr.

Jerry Neff of Battelle in Duxbury, MA shared insights and data from Australian coral

toxicity experiments.

Ms. Lori Harris and Ms. Vicki Loe of NOAA/OR&R worked hard to make this document

readable (to the extent that the material would allow) and pleasing to the eye (ditto).
TABLE OF CONTENTS

Introduction................................................................................................................................................1

Exposure Pathways..................................................................................................................................2

Coral Reef Spills, Associated Field Studies, and Large-Scale Experiments........................8

Actual Spills..................................................................................................................................9

Large-Scale Field Experiments........................................................................................... 19

Acute Effects............................................................................................................................................ 23

Chronic Effects....................................................................................................................................... 32

Behavioral Endpoints............................................................................................................. 34

Fecundity and Reproduction.............................................................................................. 39

Effects to Larvae and Larval Development................................................................... 40

Histological Changes............................................................................................................. 43

Calcification and Growth (Extension) Effects............................................................. 43

Surface Cover.......................................................................................................................... 46

Photosynthesis......................................................................................................................... 47

Mucus and Lipids..................................................................................................................... 49

Other Effects of Oil: Bioaccumulation.......................................................................................... 51

Indirect Impacts...................................................................................................................................... 55

Variability in Impact due to Reproductive Strategy ................................................................. 57

Variability in Impact with Time of Year and Region................................................................ 58

Variability in Impact with Species.................................................................................................... 60

Synergistic Impacts................................................................................................................................ 62

Summary ................................................................................................................................................... 64

Laboratory Studies................................................................................................................. 64

Field Studies.............................................................................................................................. 66

Acute Effects............................................................................................................................. 67

Chronic Effects........................................................................................................................ 67

Implications for Spill Response and Planning............................................................... 68

References................................................................................................................................................ 71

Appendix A: Glossary/Acronyms.................................................................................................... 81

Appendix B: Coral Species Citation List...................................................................................... 84

Appendix C: Coral Reproductive Type and Timing, by Region.......................................... 87

List of Figures and Tables

Figure 1. A suggested protocol or framework for initiating studies to measure

oil spill damage on corals (from Fucik et al. 1984)......................................................................7

Figure 2. Fluctuations of oil concentrations measured by fluorescence

spectrometry during 24-hr dosing for physically dispersed oil; nominal

concentrations was 20 ppm. From Knap et al. (1983).......................................................... 38

Figure 3. Accumulation (during 7-hr exposure to spiked WSF of South

Louisiana crude oil) and elimination (following return to clean seawater) of

14C-naphthalene by Oculina diffusa. From Neff and Anderson (1981)......................... 54
Table 1. Concentrations of Iranian crude oil in ml/L added to medium at start,

fatal to 0, 50, and 100 percent of Heteroxenia colonies under static and

continuous flow conditions, from Cohen et al. (1977).......................................................... 27

Table 2. Measured (by infrared spectrophotometry) replicate concentrations

of 100-percent solutions of water-accommodated fractions of test oils used

in coral toxicity experiments. Concentrations in μg/L (ppb). From Gardiner

 and Word (1997)................................................................................................................................. 32

Table 3. Stress responses shown by corals exposed to oil and oil fractions

(adapted from Fucik et al. 1984) ..................................................................................................... 36

Table 4. Range of oil concentrations (ppm, nominal) at which impairment in

specified parameter was noted in 50 percent of test colonies, by species

(Lewis 1971)............................................................................................................................................ 37
TOXICITY OF OIL TO REEF-BUILDING CORALS:

A Spill Response Perspective

INTRODUCTION

Evaluation of oil toxicity in general is not a simple or easy task. What we

consider as “oil” includes qualitatively and chemically very different kinds of

materials. Moreover, different species and even different life stages within the

same species can react in dramatically different ways to oil exposure. Because

the conditions encountered at each spill present a unique set of physical,

chemical, and biological circumstances, it is a daunting undertaking to provide

general oil toxicity guidance for responders. In the case of oil toxicity as it

relates to corals and coral reefs, it is further complicated because there is

limited information on the fundamentals of toxicity and toxicology. There is

also reasonable doubt about how well information for one area or one

species extends across other areas and the hundreds of species currently

delineated.

For spill responders and resource managers faced with making choices during

oil spills in coral reef areas, the major dilemma is how to use the available

science in a meaningful and appropriate fashion. That is, just because

someone has studied oil and corals either in the laboratory or in the field

does not necessarily mean that the results of that work will help us

understand what will occur during a specific spill or cleanup.

The several reviews on oil toxicity and effects to corals are excellent

syntheses of the state of knowledge, particularly at the time of their

preparation—which is to say, some of these reviews are dated. Loya and

Rinkevich (1980), for example, remains a good, well-referenced summary of

oil impacts. Knap et al. (1983) provided background information and a

summary of study results. Ray (1981) also included a summary of actual

incidents along with laboratory results, and then extracted lessons for

response and mitigation. A nicely illustrated overview with a solid foundation

in the literature was produced for the International Petroleum Industry

Environmental Conservation Association (Knap 1992). Neff and Anderson

(1981) not only reviewed the literature on oil impacts to a wide range of

organisms that included corals, but also performed a series of their own

experiments to augment the knowledge base. More general in scope, but

useful in providing a broader frame of reference against which oil effects can

be evaluated, are the reviews of Peters et al. (1997), Dubinsky and Stambler

(1996), and Brown and Howard (1985). Fucik et al. (1984) approach the topic

more pragmatically by focusing on damage assessment, recovery, and

rehabilitation of corals impacted by oil.
2

Those reviews attempting to synthesize the many results into coherent

lessons or themes about the effects of oil in corals often express a level of

frustration over the many challenges related to the task.

The recognition of a large range of stress responses shown by coral

is complicated by the range of oils, oil fractions, and bioassay

methodologies used in laboratory studies to date. Consequently,

identification of trends or patterns of acute or sublethal responses of

corals exposed to oil is difficult

Fucik et al. (1984)

...extrapolation of...experimental results to the field is hampered by

the unnatural spatial scale and duration of the manipulations, and

because laboratory and field experiments were not designed to

mimic real oil spills.

Keller and Jackson (1993)

The universe of available studies can also be confusing because they often are

contradictory: some research indicates serious impacts to corals while others

conclude few, if any, consequences of oil exposure. Some coral toxicity

reviews critique other reviews. For example, one summary by Johannes

(1975) asserted that “...there appears to be no evidence that oil floating above

reef corals damages them,” but Marshall et al. (1990) pointed out that the

studies that led Johannes to this conclusion were largely anecdotal and did not

include consideration of sublethal or longer-term effects.

How, then, do we sort through the literature and available science to glean

lessons of relevance and utility for spill response? One strategy is to overlay

the framework of each study on expected scenarios for actual spills. For

example, one parameter that could be evaluated in this way is the nature of oil

exposure to test corals in various studies. How did the oil come into contact

with the animals? Corals, of course, reside (mostly) in the subtidal, while oil

(mostly) floats. What is the best way to simulate the exposure corals might

experience during an oil spill? As Ray (1981) commented in his review of oil

effects in coral, “Oil preparation and exposures ran the entire gamut...Some

of these techniques may simulate actual field exposures, others are

unrealistic.” Therefore, the pathway becomes an important consideration in

the process of understanding coral toxicity.

EXPOSURE PATHWAYS

The means by which corals can be exposed to oil has a direct bearing on the

severity of resultant impacts. Three primary modes of exposure can be

envisioned for coral reefs in oil spills. In some areas (especially the IndoPacific), direct contact is possible when surface oil is deposited on intertidal

corals. Presuming that some portion of spilled oil will enter the water
3

column either as a dissolved fraction or suspended in small aggregations, this

potential pathway must be considered in most cases. Subsurface oil is a

possibility in some spills, particularly if the spilled product is heavy, with a

density approaching or exceeding that of seawater, and if conditions permit oil

to mix with sediment material to further increase density.

Evaluation of risk based on exposure pathway is a complex calculus that is

highly spill-dependent. Relevant questions that feed into the determination

are linked to the considerations above:

• Are corals in the affected area intertidal?

• Does the spilled oil have a lighter, more water-soluble component?

• Will sea conditions mix oil on the surface into the water column?

• Is there a heavier component to the oil that raises the possibility of a

density increase through weathering and association with sediment that

could make the oil sink?

Areas where corals are intertidal in distribution could be considered to be at

greatest risk in a spill because of the increased potential for direct contact

with a relatively fresh oil slick. Regardless of differences in susceptibility by

species or physical form, direct oil contact is most likely to result in acute

impact. In this kind of exposure the dose is very high and impacts from

physical coating are an added mechanism of toxicity.

Coral exposure via the water column could be a serious route under some

circumstances. Because many of the components in oil have a relatively low

solubility in water, in general coral may be protected from exposure by

overlying waters. However, if rough seas and a lighter, more soluble product

are involved, subtidal corals may be harmed by exposure to enhanced

concentrations of dissolved and dispersed oil. The absolute levels of

exposure would be expected to be much lower than those experienced by

direct contact with intertidal slicks, since only a small fraction of the total oil

can be placed into the water column either in solution or physically

suspended. However, the components of the oil most likely to enter the

water column are those generally considered to have the highest acute

toxicity. Corals may therefore be exposed to “clouds” of dispersed oil driven

into the water column under turbulent conditions, with impacts dependent on

exposure concentrations and length of exposure.

Heavier fuel oils contain fewer of the light fractions identified with acute

toxicity than refined and crude oils (although these bunker-type oils are

sometimes “cut” with lighter materials to meet customer specifications for

viscosity). If they remain on the water surface, spills of heavier fuel oils are

less of a concern from a reef perspective, and perhaps more of a concern for
4

protection of other habitats like mangrove forests where they can strand and

persist for long periods of time. However, the heavy oils can also weather or

be mixed with sediments and increase in density to the point where they may

actually sink—providing a direct route of exposure to subtidal habitats and

corals. Although acute toxicity characteristics of heavy fuel oils may be lower,

the potential for significant physical effects from smothering is greatly

increased.

Examining how laboratory exposure methods compare to those likely to be

encountered in situ reveals that a fundamental limitation—for our purposes

here—of many of the available research studies on the effects of petroleum

compounds on corals is that they rely on nominal rather than measured

exposure concentrations. What this means is that the researchers frequently

have reported oil exposure concentrations based on the proportions of oil

added to water only, and did not actually measure how much of that oil was

ultimately mixed into the water as a source of exposure to tested coral

colonies.

Why is this problematic? There is likely to be a vast difference between a

nominal concentration of oil in water of, say, 100 parts per million (ppm) and

the amount that is actually dissolved or accommodated into the water column

after mixing: the latter is probably lower by 1-2 orders of magnitude or more.

What this means is that in studies where only nominal concentrations are

reported, the actual effects levels are much lower than those reported.

While nominal concentrations still permit reasonable comparison of effects

at different levels within a given study, they make it almost impossible to

generalize about or compare effects levels across studies. This significantly

reduces our ability to extrapolate experimental results to a spill scenario.

It is not a new lament and, in fact, this weakness has characterized oil toxicity

studies in general for many years. In their review of oil effects studies in the

reef environment, Knap et al. (1983) list it as one of the primary difficulties in

interpreting the results of available biological investigations.

Further complicating the task of understanding or predicting oil spill impacts

in coral reefs based on the experimental literature is the fact that typical reallife exposures are unlikely to be constant. That is, most oil and coral studies

are based on exposures to a certain concentration for a certain period of

time. This is a standard approach in toxicology. In contrast, an oil spill,

whether or not it is dispersed, probably would be characterized with highest

exposure concentrations of hydrocarbons at the very beginning of the incident

when the product is relatively consolidated in one location and relatively

unweathered. This peak exposure could then be expected to decline rapidly

and steadily as the spill spread laterally and weathering processes began to

change the composition of the mixture. Of course, in a real spill there could

be special circumstances (e.g., stormy conditions, intertidal stranding of large
5

amounts of oil, sinking oil) that would alter the expected behavior and

exposure of the oil; but the pulsed character of exposure is a reasonable

scenario for a generalized spill.

This type of exposure scenario is more difficult to simulate in the laboratory

than a constant exposure over a given experimental period. Some

researchers model it by removing oil from the experimental system after an

amount of time defined to be consistent with the amount of time a slick might

reside on the water in an affected area. Others, especially those studying the

effects of dispersed oil, introduce a pulse of oil into a flow-through system

that is then allowed to dissipate with time. There is no question that

methods have become more refined over the years to more realistically

portray conditions in a spill, but results must still be interpreted and

compared with caution.

This being said—even with the limitations of nominal concentrations and

variable and unrealistic exposure conditions that were especially common in

earlier coral and oil toxicity investigations, the available results still provide a

relatively good survey of the kinds of impacts that might be expected when

corals are exposed to oil. Although absolute threshold levels often cannot be

derived from the studies, a suite of fundamental oil effects to corals emerges

that can serve as the basis for anticipating potential impacts during a spill.

In this report, we intend to present an overview of known toxicity

information for oil and corals. Although it will become apparent that a wide

range of impacts has been documented over the years, certain patterns and

consistencies emerge that we highlight as toxicity “common threads.” The

focus of our discussion is intentionally narrow, i.e., oil effects on corals

themselves and not on the associated reef community of plants and animals.

This was necessary to establish some reasonable bounds on the survey and

synthesis effort, although we recognize and acknowledge that doing so

arbitrarily and artificially limits the assessment of spill effect.

Many others have commented on the interrelated nature of reef

communities. In their review of oil spill damage, recovery, and rehabilitation

in coral reef systems, Fucik et al. (1984) point out that the discussion of

criteria for the assessment of damage and recovery in coral systems must

draw the distinction between the coral component alone and the total reef

ecosystem. Coral reefs are almost universally recognized as highly productive

and sensitive systems. Fucik and colleagues noted that although the

hermatypic corals ultimately provide the fundamental structural framework

for the entire reef, the coral organisms themselves do not necessarily

dominate the biomass, productivity, or calcification. Brown and Howard

(1985), in discussing assessment of stress in reef systems, pointed out some

of the problems in isolating the corals themselves from the reef dwellers

during such a process. They noted that, following a hurricane in St. Croix,
6

scleractinian coral diversity decreased in shallow waters, but diversity of the

community as a whole actually increased due to the colonization of new

substrate by a wide range of organisms. Their conclusion: “Clearly

quantitative measurements on coral reefs affected by disturbance should

include some account of all major components of the reef community.”

In an ideal world, we would take that advice (of course, in an ideal world,

there would be no oil spills). It seems logical that impact assessment in coral

reef systems should ideally include the associated community of plants and

animals, to acknowledge the ecological linkages and portray a realistic set of

spill-related conditions. Realistically, however, that comprehensive approach

would enormously complicate the task at hand. Because of the basic role the

corals play in the overall reef systems, and because a large-scale impact to the

coral component would subsequently affect all associated plants and animals,

Fucik et al. suggested that the initial focus in assessing oil spill impacts should

be on the corals themselves. Therefore, for this and the pragmatic reason

above, we have intentionally chosen to restrict ourselves to corals only in this

review.

Similarly, we have not included a comprehensive review and discussion of the

literature on chemical dispersants, chemically dispersed oil, and corals.

There have been a number of efforts to compare the relative toxicities of oil,

dispersants, and dispersed oil to corals. These are summarized elsewhere

(see, for example, Hoff 2001). In our review here, we focus on the toxicity

information for oil alone, isolating these results from others where possible

and appropriate. In some cases, where oil and dispersant data are integrated

or the oil-only data difficult to extract from a study, the dispersant results are

included as well.

Fucik et al. provided a framework for assessing oil-related damage in a coral

reef system(Figure 1). They noted the inherent problems in providing input

into this framework, such as community level impacts are most severe but

the most difficult to quantify accurately, while organismal impacts can be

easier to measure but provide the least information on assessing the overall

significance of perturbations on an ecosystem. Nevertheless, their decision

tree provides a relevant example of how scientific support personnel in a spill

setting could use on-scene observations along with the known science to

provide at least some level of guidance. To the protocol Fucik et al.

suggested in 1984, we might add additional considerations of sub-organismal

levels of consideration such as cellular or even genetic impacts. Recently

developed approaches, which will be alluded to later, may provide additional

ways to assess impact to reef systems and isolate spill-induced damage from

other stressors.
7

Are massive mortalities

evident on the reef?

Are changes in physiological

parameters of individual

organisms evident on a broad

scale (e.g., reduced growth &

reproduction)?

Damage is probably minimal

or unmeasurable.

Is the structure of the reef

community changing?

Recovery will probably be

short-term.

Are functional components

of the reef affected?

Significant damage due to

loss of productivity; recovery

of reef may be impossible.

Significance of damage is

dependent on degree of

structural change and species

affected; reef may or may not 

recover to original state.

NO

NO

NO

YES

YES

NO YES

Organismal

Structural

Functional

Figure 1. A suggested protocol or framework for initiating studies to

measure oil spill damage on corals (from Fucik et al. 1984).
8

Our discussion of oil toxicity to corals is organized in the following manner.

First, we summarize the known spills in coral reef areas and describe largerscale field experiments. Next, we review documentation of acute toxicity. A

section follows this on chronic toxicity effects, a generally well studied subject

area that we have chosen to subdivide into categories of effect for purposes of

organization. Next, we present individual summaries of information on

bioaccumulation, indirect impacts, the influence of reproductive strategy,

variability in effect with time and location, species differences, and synergistic

effects. These are interpreted with a spill- response orientation to highlight

relevant issues during an incident. Finally, we end with some “bottom line”-

type insights and advice for responders and resource managers.

CORAL REEF SPILLS, ASSOCIATED FIELD STUDIES, AND

LARGE-SCALE EXPERIMENTS

In theory, studies of actual spills in coral reefs should provide the

best information on oil impacts in this habitat. In reality, these have

been less than illuminating because they are infrequent and often

confounded by other sources of disturbance in the reef

environment. Of eleven coral reef spill studies cited here, four

concluded that little damage occurred, two concluded that major

damage occurred, and five neither explicitly nor adequately

described effects to the coral reefs themselves.

In theory, large-scale field studies should offer the next-best setting

in which to assess oil impact. In reality, these are difficult and

expensive to undertake, and thus, even more scarce than spill

studies. The two field experiments referenced here indicated little

short- or long-term impact of exposure conditions typical of spills.

Case studies of actual oil spill events offer the best opportunity to investigate

the effects of oil in a coral reef environment. However, these are also

limiting, for at least two reasons: first, despite the seemingly increased risk

posed by proximity to major shipping lanes, a relatively small number of

major spills have taken place around coral reefs; and second, those spills

known to have occurred near coral have not been well-studied. This is

especially true for earlier (1960s and before) incidents.

In the absence of an actual oil spill incident, a large- or realistically scaled

experimental spill offers an excellent—and, in some ways,

better—opportunity to study oil spill impacts to coral reefs. The advantages

are the ability to adequately prepare for impact assessment and the enhanced

ability to control potentially confounding external parameters. Disadvantages

include the reluctance of most environmental regulators to permit the

intentional release of a pollutant, regardless of containment; and a significant

degree of logistical support (translation: $$) necessary to implement a well-
9

designed and monitored experiment of this kind. Though these studies are

even rarer than coral reef spill assessments, two of them are described

below.

ACTUAL SPILLS

Argea Prima, Puerto Rico

July 1962

On the evening of July 16, 1962, the Italian tanker Argea Prima ran aground off

Guayanilla Harbor on the southern shore of Puerto Rico. In an attempt to

lighten the vessel to free it from the rocks, the captain decided to pump about

72,200 bbl (11,481,000 L) of crude oil into the sea. The oil was blown ashore

and transported by currents far to the west. Diaz-Piferrer (1962). is the only

published account of this spill that we could find. Diaz-Pifferer had maintained

a study site at Guánica before the spill, and so was well positioned to describe

changes following the spill. As reported by Diaz-Pifferer, those changes were

significant: the physical character of the beaches shifted dramatically and, in

some places, all sand was washed away when it formed aggregations with oil

and was washed away in the surf*

; mangroves habitat in the affected zone was

“virtually destroyed” by large amounts of oil; and a widespread and heavy

mortality of nearshore animals was described, including adult and juvenile

lobsters, crabs, sea urchins, starfishes, sea cucumbers, gastropods such as

king helmets and queen conchs, octopi, squids, a variety of fishes (particularly

clupeoids), and sea turtles. Large areas were denuded of algae, and sea grass

beds (Thalassia) were “badly affected.”

Although Diaz-Piferrer noted that coral reefs west of the grounding site were

initially thickly covered with oil, there was no subsequent discussion of either

short-term or long-term impact to corals.

Brother George, Dry Tortugas, Florida

January 1964

In January 1964, the tanker Brother George spilled 3,610 bbl (573,944 L) of

unidentified oil near Bird Key Reef, in the Florida Keys. Jaap et al. (1989)

noted that only cursory studies of reef damage took place at that time and

thus it is unknown if the oil damaged colonies of Acropora palmata there.

This short account was the only published documentation of this incident

found, and no further details are available.

 

*

 An oil geomorphologist who reviewed this manuscript argued that this erosional mechanism

attributed to oiling is not possible.
10

R.C. Stoner, Wake Island

September 1967

On September 6, 1967, the 18,000-ton tanker R.C. Stoner attempted to moor

to two buoys when strong winds drove the vessel aground 200 m southwest

of the harbor entrance at Wake Island. The only documentation of this

incident is found in Gooding (1971).

The tanker was fully loaded with over 142,857 bbl (22,712,500 L) of refined

fuel oil products. This included 83,500 bbl (13,275,400 L) of JP-4 aviation jet

fuel; 42,500 bbl (6,756,960 L) of A-1 commercial aviation fuel; 10,000 bbl

(1,589,870 L) of 115/145 aviation gasoline; 4,000 bbl (635,949 L) of diesel oil;

and 3,300 bbl (524,658 L) of Bunker C. There was an immediate release of

fuel after the grounding, believed to be primarily aviation gas, JP-4, and A-1

turbine fuel. On the following day, a “considerable quantity” of Bunker C was

also observed, and gasoline vapor odor was detected through September 8.

The heavy cargo load and rough seas hampered efforts to refloat the vessel,

and on September 8 the stern of the ship broke off. An estimated 14,286 bbl

(2,271,250 L) of the mixed fuels covered the surface of a small boat harbor, up

to 20 cm thick. The strong southwest winds concentrated the spilled oil in

that harbor and along the southwestern coast of Wake Island, which consists

of three islets forming an atoll enclosing a shallow lagoon. Large numbers of

dead fish were stranded along this shoreline. Oil recovered from the small

boat harbor by pumps and skimmers was moved into pits near the shore and

burned each evening; over 378,541 L were disposed of in this fashion. The oil

was blocked from entering the central lagoon area of the Wake Island group

by an earthen causeway.

The Federal Aviation Administration (FAA) cleared dead fish from the

shoreline area closest to the spill location. In addition to the massive fish kill

(approximately 1,360 kg collected), dead turbine mollusks, sea urchins, and a

few beach crabs were also reported. About 2.4 km of shoreline beyond the

FAA-cleaned zone was also oil contaminated, and Gooding estimated that

another 900 kg of dead fish were not removed. Other dead invertebrates

(cowries, nudibranchs, grapsoid crabs) were also observed.

In this assessment, corals in the area were mentioned only in passing, and

apparently were not surveyed either formally or informally for impact.

Discussion of corals was completely in the context of the associated fish

communities. Given the mixture and quantities of fuel spilled, and the

massive mortalities manifested in fish and reef-associated invertebrates, there

almost certainly was an impact to the coral animals themselves. Gooding did

note that, on a survey conducted 11 days after the grounding, the only

remaining visible impact in the inner harbor was black oil impregnated in

coral. He stated that only cursory observations were made on reef

invertebrates and, given external challenges to impact assessment described in
11

the account (typhoons, tropical storm, harassment by black-tipped sharks,

skin irritation to divers from exposure to fuels in water), effects to coral

were presumably not included in survey objectives.

Ocean Eagle spill, Puerto Rico

March 1968

Morris J. Berman, Puerto Rico

January 1994

These two spills are grouped here and summarized primarily because they

were similar in two respects: their location, along the northern shoreline of

Puerto Rico, and the lack of reported impact to coral reefs. The two

considerations are linked. The northern coast of Puerto Rico has many large

hotels and recreational beaches, but few coral reef areas.

The circumstances of the two spills were otherwise rather different. The

Ocean Eagle grounded on March 3, 1968 in San Juan Harbor, after which it

broke in two and spilled 83,400 bbl (13,259,500 L) of Venezuelan light crude

oil (NOAA 1992). The Morris J. Berman was a barge laden primarily with No.

6 fuel oil and drifted ashore about 300 m off Escambron Beach after its towing

cable parted on January 7, 1994 (NOAA 1995).

Impacts of concern, as noted above, were similar. Nearly all of the large

tourist hotels and beaches in San Juan are concentrated along the northcentral shoreline of Puerto Rico, where much of the oil in both incidents

came ashore. Although many of these recreational areas were heavily

impacted, sensitive natural resources such as coral reefs and mangroves that

would be a major concern elsewhere in Puerto Rico, are not abundant here.

Widespread mortalities, primarily among fish and benthic invertebrates, were

noted during both the Ocean Eagle (Cerame-Vivas 1968) and the Morris J.

Berman (NOAA 1995) spills; however, there is no mention of adverse effects

to corals in either case.

SS Witwater spill, Panama

December 1968

On December 13, 1968, the 35,000 bbl (5,564,560 L) tanker SS Witwater

broke apart on the Caribbean coast of Panama and released around 20,000 bbl

(3,179,750 L) of Bunker C and marine diesel oil. The spill occurred within 5.5

km of the then-new Smithsonian Tropical Research Institute laboratory at

Galeta Point.

The incident highlighted the dearth of baseline information on Caribbean

intertidal reef flat communities, and the Smithsonian lab invested a substantial

effort to compile those data. These data provided background information

for experimental tests of effects of oil, reported in Birkeland et al. (1976).
12

Rützler and Sterrer (1970) did report on damage to tropical communities,

including corals, from the spill. They referred to the recent, incomplete

baseline surveys of unimpacted communities, but based their assessment of

actual and potential damage on comparisons with data from other areas in the

tropical Atlantic.

The authors reported that coral reefs, consisting mainly of Porites furcata, P.

asteroides, Siderastrea radians, and Millepora complanata (a hydrocoral), seemed

to be the least affected of all the communities studied. At the time of the

survey (2 months after the spill), no ill effects were observed. Rützler and

Sterrer attributed this lack of impact to the subtidal nature of the reefs (i.e.,

lack of direct contact) and a higher than normal low tide caused by high winds.

Tarut Bay, Saudi Arabia

April 1970

During a storm on April 20, 1970, a pipeline broke on the northwest shore of

Tarut Bay in Saudi Arabia. An estimated 100,000 bbl (15,898,700 L) of Arabian

light crude oil entered the shallow bay. The spill was briefly documented in

Spooner (1970), who described the cleanup actions (which included the use of

the chemical dispersant Corexit 7664), and the initial mortalities of intertidal

invertebrates (crabs and mollusks), fish, and one rat. Oiling was noted on

dwarf mangroves and three months later some of these trees died. Spooner

did not describe any impacts of the spill on coral reef areas, although she did

comment that in a shallow (2.5-4.6 m) area of Tarut Bay directly east of the

pipeline break area, an area of Acropora sp. was found “...growing healthily

with abundant and diverse associated fauna...in an area which had been

subjected to potential oil pollution from effluent and from terminal accidents

for the past 25 years.” This seemingly implied that the coral was not

particularly sensitive to either the acute exposure of the pipeline spill or the

chronic exposure of proximity to normal bulk loading.

T/V Garbis spill, Florida Keys

July 1975

On July 18, 1975, the tanker Garbis spilled 1,500 to 3,000 bbl (238,481 to

476,962 L) of crude oil into the waters approximately 48 km SSW of the

Marquesas Keys, Florida. The oil was blown ashore along a 56-km stretch of

the Florida Keys, east of Key West. The only published description of this

spill and its impacts are found in Chan (1977), although the 1976 M.S. thesis of

that author at the University of Miami in 1976 further detailed effects and

recovery. The source of the spill, the Garbis, was identified after the

publication of both documents (E. Chan, pers. comm., 2000).

In addition to documenting early impacts, Chan established a series of sites to

be monitored over a longer period of time (a year). Since no pre-spill
13

information was available, effect and recovery were judged through

comparison with unoiled, biologically similar locations.

Several habitats were impacted and described. Some of the impacts were

severe, e.g., mortalities in echinoderms and pearl oysters. However, a

notable lack of spill effect was found in coral reef areas. Reefs were surveyed

by divers immediately following the spill and subsequently in August and

November 1975 and January 1976. Chan attributed this lack of impact to the

fact that the reefs were completely submerged during the spill, and to calm

seas that minimized water column contact with the oil.

Peck Slip, Puerto Rico

December 1978

On December 19, 1978, the barge Peck Slip was damaged in heavy weather in

the Pasaje de San Juan along the eastern side of Puerto Rico. Approximately

10,476-10,952 bbl (1,665,580-1,741,290 L) of Bunker C oil were discharged

while the barge was towed to Puerta Yabucoa, its original port of departure.

Gundlach et al. (1979) and Robinson (1979) reported that four habitats were

surveyed for possible damage from the spill: sand beaches, gravel/cobble

beaches, mangrove forests, and offshore lagoons and coral reefs. Although

26 km of shoreline was oiled, most of the oiled areas were sand beaches.

Diver surveys of coral reef areas did take place; despite some evidence of oil

in bottom sediments, Gundlach et al. reported no observed biological impacts

to this habitat.

Robinson (1979) provided more detail on the assessments that took place,

including those targeted on coral reef habitats. Diving surveys were

conducted in one area of offshore coral reefs (Río Mar). The reef types were

classified as nearshore fringing reefs and offshore patch reefs. Constituent

corals were identified as Montastrea annularis, M. cavernosa, and Diploria

strigosa. Robinson attributed the generally low diversity of corals in these

habitats to high turbidity.

Aerial observations of the reef areas showed the presence of oil and sheens

on the water. In addition sediment cores taken at offshore stations revealed

“very light oil” had been incorporated into most of the bottom sediments in

the Río Mar area. However, no oil was seen on the surface of bottom

sediments or on corals, and the observed organisms “exhibited no abnormal

behavior.”
14
15

Bahía Las Minas, Panama

April 1986

On April 27, 1986, about 240,000 bbl (38,157,000 L) of medium-weight crude

oil (70 percent Venezuelan crude, 30 percent Mexican Isthmus crude) spilled

from a ruptured storage tank at a petroleum refinery at Bahía Las Minas, on

the central Caribbean coast of Panama. Of this amount, Keller and Jackson

(1993) estimated that at least 60,000-100,000 bbl (9,539,240 -15,898,700 L)

spilled into the waters of Bahía Las Minas. According to Jackson et al. (1989),

this was the largest recorded spill into a sheltered coastal habitat in the

tropical Americas. It also happened to occur near the Smithsonian Tropical

Research Institute’s Galeta Marine Laboratory. As a result, the Bahía Las

Minas spill was extensively studied, and the results from those investigations

constitute a large part of the available field effects literature for oil impacts to

coral reef (and other tropical) communities.

The area where this spill occurred was not pristine before the 1986 incident.

Guzmán et al. (1991) pointed out that a wide range of human activities

spanning more than a century has extensively modified and degraded Bahía Las

Minas. . Nevertheless, the team of researchers studying the effects of the

Bahía Las Minas spill concluded that the incident had major biological effects in

all environments examined, including the coral reefs and reef flats.

Widespread lethal and sublethal effects were noted. In coral reefs, the cover,

size, and diversity of live corals decreased substantially on oiled reefs after the

spill. Apparent sublethal impacts included decreased growth, reproduction,

and recruitment. Keller and Jackson (1993) summarize and synthesize the

results from the large team of investigators; results from coral researchers

are cited more specifically in the discussions to follow.

Although Corexit 9527 oil dispersant was used during the initial response to

this spill, Keller and Jackson termed the overall dosage of dispersant as “low,”

and concluded that the limited use of the chemicals could not explain the

widespread subtidal biological impacts reported.

Gulf War spill, Arabian Gulf

January 1991

During the waning days of the Gulf War conflict in 1991, the Iraqi military

deliberately discharged oil, causing the largest oil spill in history, variously

reported to be between 6.3 million and 10.8 million bbl (1,001,620,000-

1,717,060,000 L). Between 19 and 28 January, 1991, oil was released from

two major sources: three Iraqi tankers anchored in the Kuwaiti port of Mina

Al-Ahmadi; and the Mina Al-Ahmadi Sea Island terminal area (Tawfiq and

Olsen 1993). Aerial fallout from the 730 oil wells destroyed by the retreating

Iraqi forces indirectly contaminated the nearby marine waters (Saenger

1994).
16
17

Given the magnitude of this release and the previous coral reef impacts noted

at other tropical spills, there were dire expectations of severe impacts to

nearshore and offshore reefs in Kuwait and Saudi Arabia. However, to date

the extent of coral reef damage directly attributable to the Gulf War spill has

been remarkably minor.

Downing and Roberts (1993) surveyed the nearshore and offshore reefs in

1992 and noted rather equivocal indications of effect in ostensibly heavily

impacted areas. For example, a reef at Qit’at Urayfijan was very likely

covered by oil released from at least one tanker and the Mina Al Ahmadi

terminal. While the reef is never exposed to the atmosphere, Downing and

Roberts stated that crude oil probably flowed over it for days. This reef was

clearly impacted, mostly in shallower water, with mortalities noted in large

colonies of Platygyra as well as in most of the Porites (Downing and Roberts

did not identify corals observed to species). New growth, however, was

observed in nearly all dead portions of coral.

In contrast, Downing and Roberts also reported on conditions at Getty Reef,

close to a visibly oiled beach and directly downstream from known release

points. Here, there was no evidence of recent coral kills or even stress

among Porites, Platygyra, Cyphastrea, Leptastrea, Psammocora, Favia, and Favites,

and the associated fish community was especially robust.

The authors do not dismiss the possibility of a spill impact on the coral reefs,

but suggest that it may be obscured by the effects of other environmental

factors. They also discussed potential indirect impacts of the conflict, such as

reduced water temperature and ambient light due to smoke cover, lasting

several days, from oil fires.

Vogt (1995) established six 50-m study transects nearshore and offshore the

Saudi Arabian shoreline to document effects and recovery from the 1991 Gulf

War oil spill. On the basis of video recordings made along these transects

between 1992 and 1994, Vogt concluded that live coral cover had significantly

increased and that the corals offshore from Saudi Arabia had survived the

largest spill on record “remarkably unscathed.”

Saenger (1994) summarized many of these same results and commented on

the contrary nature of the findings relative to expectations of damage in the

wake of the massive release. In addition to discerning no demonstrable direct

effects of oil, Saenger further noted that spawning activities of staghorn corals

(Acropora sp.) were not impaired in either 1991 or 1992. He suggested three

possible reasons for the accelerated “self-purification processes:”

• Acclimatization and proliferation of efficient, oil-degrading

microorganisms due to long periods of exposure to natural seeps and

releases;
18

• Exceptionally high ambient temperatures, which increase both rates of

volatilization of lighter fractions of oil and of intrinsic biodegradation;

• Enhanced rate of photo-oxidation due to lack of cloud cover and shallow

depths of the Arabian Gulf.

Other Gulf War spill researchers have suggested alternate explanations for

the minimal impact reported to coral reefs. For example, Michel (pers.

comm., 2001) noted that Kuwaiti crude oil has one of the highest rates of

emulsification of any crude and combines with water to form a very stable

emulsion (cannot be broken with chemicals, heat, or re-refining). The rapid

and persistent emulsification may well have prevented most of the oil from

entering the water column to harm corals. Moreover, the Arabian Gulf is a

low-energy system, so there would be little mixing of oil into the water

column.

Whatever the causes or conditions responsible for the noted lack of adverse

effect, Saenger cautioned that these and other unique conditions found in the

Gulf region suggested that extrapolating oil impact (or lack thereof) to other

areas, such as the Great Barrier Reef, was probably not appropriate.

Rose Atoll National Wildlife Refuge, American Samoa

October 1993

On October 14, 1993, the Taiwanese fishing vessel Jin Shiang Fa ran aground

on the southwestern side of Rose Atoll, a remote coral reef in eastern

American Samoa. In 1974, Rose Atoll was designated as a National Wildlife

Refuge because of its fish and wildlife resources, which include giant clams and

green sea and hawksbill turtles. The grounding spilled 2,381 bbl (378,541 L)

of diesel fuel and other materials (lube oil and ammonia) onto the reef.

Previously, this had been considered one of the most remote and pristine

coral reefs in the world. Green et al. (1997) consolidated information and

performed impacts assessments for the U.S. Fish and Wildlife Service, which

administers the National Wildlife Reserve.

Rose Atoll is a unique coral habitat in Samoa, in that crustose coralline algae

(identified as primarily Hydrolithon onkodes and H. craspedium) dominate

instead of the hermatypic corals. The reef-building corals are present; Green

et al. list Favia, Acropora, Porites, Montipora, Astreopora, Montastrea, and

Pocillopora as being the common genera.

All of the petroleum products and ammonia were released into the marine

environment over a period estimated as six weeks. Wave action reportedly

mixed oil and oily debris from the wreck down onto the reef structure.

Although the injury to the corals from the grounding was judged to be

“moderate to high,” it was not possible to ascertain causal factors in a more

specific way. Several possible injury pathways were identified:
19

• Fuel and other contaminant toxicity;

• Mechanical damage from the grounding and subsequent debris impacts;

• Anoxia due to mortalities in the reef community;

• Smothering and scouring from sediments created by the wreck;

• Competition from opportunistic algae; and,

• Bleaching from direct and indirect impacts of the incident.

While the physical effects of the grounding were obvious and long-term, the

authors contend that the most widespread and severe injuries to the atoll

seemed to be due to the release of diesel fuel. A massive die-off of coralline

algae and many reef-dwelling invertebrates was observed after the release;

blue-green algae blooms were recorded where they are typically not found;

and the structure of algal communities had shifted substantially. Four years

after the grounding, the affected areas remained visibly impacted—particularly

with respect to coralline algae cover—and Green et al. cast some doubt as to

whether Rose Atoll would ever return to its former pristine condition.

Review of these case studies does not yield a preponderance of evidence

either for or against a finding of oil spills consistently causing damage to coral

reefs. Some of the early spill accounts might be discounted as coral effects

benchmarks, since the corals themselves did not appear to be high priorities

for injury assessment when those studies took place. However, the more

recent and intensively studied spills in Panama (Bahía Las Minas) and the

Arabian Gulf (Gulf War) yielded one conclusion of moderate to severe

damage, and one of little to no damage, respectively. Perhaps the one truism

that emerges is that the unique characteristics of oil spills do not permit

extrapolation very far beyond the individual circumstances of each incident.

LARGE-SCALE FIELD EXPERIMENTS

Tropical Oil Pollution Investigation in Coastal Systems (TROPICS),

Panama

December 1984; September-November 1994

In 1984, the American Petroleum Institute (API) sponsored a multi-year

experiment in which a representative tropical system (comprised of

mangrove, seagrasses, and coral) was exposed to oil and chemically dispersed

oil. The experimental design was intended to simulate a severe, but realistic,

scenario of two large spills of crude oil in nearshore waters. Ballou et al.

(1987) detailed the original experiment and its findings.

In 1994, the Marine Spill Response Corporation (MSRC) and API sponsored a

revisit to the experimental site by much of the original research team. The

findings from the ten-year follow-up studies were published as Dodge et al.

(1995).
20
21

Although both efforts encompassed oil and chemically dispersed oil effects

studies in mangrove, seagrass, and coral systems, only oil in corals will be

discussed here. The reader is directed to the referenced documents for

information and details on the other study components.

The sites selected for the experiment were located on the Caribbean coast of

Panama, in northwestern Laguna de Chiriqui. The area was extensively

surveyed, and experimental sites were chosen based on suitability of the

three habitat types to be studied. Porites porites and Agaricia tennufolia

dominated coral reefs. Ultimately, three sites (oil, dispersed oil, and

untreated reference) were selected. The oiled site was treated with 953 L of

Prudhoe Bay crude oil, which was released onto a boomed area of the water

surface and allowed to remain for about two days. Tides and winds

distributed the oil over the study area. After the exposure period free-floating

oil was removed with sorbents.

Chemical monitoring of water exposure was extensive, using continuous

fluorometry, fixed-wavelength ultraviolet fluorometry, and discrete water

samples analyzed using gas chromatography (GC), and mass spectrometry

(MS). The continuous fluorometry indicated mean exposure (hourly

averages) of 1.4 and 2.5 parts ppm under the slick. Discrete water samples

taken during the oiling treatment and analyzed by GC and GC/MS showed low

exposure levels ranging from 0.01 to 0.09 ppm. Targeted analyses for low

molecular-weight hydrocarbons ranged between 33 and 46 parts per billion

(ppb), which was about two orders of magnitude less than levels at the

chemically dispersed study plots.

For coral reefs, detailed transects measured abundance of epibiota living on

the reef surface. Four measurements were taken: total organisms, total

animals, total corals, and total plants. Growth rates of four coral species (P.

porites, A. tennufolia, Montastrea annularis, and Acropora cervicornis) were also

measured.

Of all the parameters listed above, the only statistically significant effect

documented over the first 20 months at the oiled site was a decrease in coral

cover. No significant changes in growth rates of the four targeted corals were

noted.

The follow-up survey in 1994 showed no significant consequences to coral

cover or coral growth. The authors contrasted the finding of no impact from

oiling alone to that described by Guzmán et al. (1991) at Bahía Las Minas,

where significant effects of oil alone were found in several of the same species

studied at TROPICS. Dodge et al. implied that the greater damage may have

been due to the size of the spill and continued chronic exposure at Bahía Las

Minas.
22

Arabian Gulf field experiment

September 1981-September 1982

LeGore et al. (1983; 1989) described a large-scale field experiment carried

out on Jurayd Island, off the coast of Saudi Arabia in the Arabian Gulf. The

authors acknowledged the inconsistency in the scientific literature regarding

oil impact on corals, and pointed out that much of the literature consisted of

opportunistic observation of uncontrolled oil spills or controlled laboratory

experiments under artificial and unrealistic conditions. They offered their

experimental design and its results as a response to the stated need for more

realistic toxicity testing and field verification of lab test results.

The study was designed to determine responses of corals to dispersed oil

under realistic spill conditions, but the design included exposure to crude oil

only (Arabian light) among its four exposure scenarios. Two exposure time

periods were selected: 24-hr, and 120-hr. Study plots were established over

coral reefs comprised mostly of Acropora spp. (more than 95 percent), with

scattered colonies of Platygyra sp., Goniopora sp., and Porites sp. The plots

measured 2 m x 2 m, located over approximately 1-m depth at low tide, and

anchored in place. These were surrounded by oil-containment boom

measuring 7.5 m x 7.5 m. Two plots were established for each treatment.

The stated intent of the experiment was to simulate conditions of a typical

Arabian Gulf oil spill and not to overwhelm the corals with “extraordinary

and catastrophic stresses.” As such, oil was added to test plots to produce a

slick of 0.25 mm thick, a total of 14 L in the 24-hr oil only treatment; and 0.10

mm and 5.63 L in the 120-hr experiment. Water concentrations of

hydrocarbons were measured by infrared methods, and all measurements

were below detection limits in the oil-only plots.

The oil-only plots were visually inspected at the end of the 24-hr and 120-hr

exposures, and they appeared normal. These areas were monitored for one

year, and no extraordinary changes occurred relative to the unoiled plots

(seasonal changes in degree of bleaching, however, were noted across all

monitored plots). While dispersed oil appeared to delay the recovery from

seasonal bleaching, this was not observed in the oil-only plots.

Growth rates, expressed as skeletal extension along branch axes, showed no

correlation to treatment in the 24-hr exposure. There was some indication

that growth rates were depressed with 120-hr exposure, but LeGore et al.

cautioned that these were not definitive.

The authors made the following conclusions:

• No visible effects were exhibited over a 1-year observation period by

Arabian Gulf corals exposed to floating crude oil corresponding to a slick

thickness of 0.25 mm.
23

• Corals exposed for 5 days to floating crude oil corresponding to a slick

thickness of 0.10 mm exhibited no visible effects during the 1-year

observation period.

• Coral growth and colonization of study plots appeared unaffected by

exposure to crude oil in both the 1-day and 5-day experiments.

• There was a similar lack of impact in dispersant and dispersed oil

experiments, although corals exposed to dispersed oil for 5 days showed

some delayed stress reactions and possibly some synergistic impacts from

cold winter temperatures.

There were few observed effects in the two large-scale field experiments that

have examined oil and corals. With only two studies of this type available,

generalizations can be made only cautiously. What these experiments do

show is that it is possible to have realistic exposure scenarios with oil on the

water over coral reefs and have few, if any, demonstrable impacts. However,

they do not rule out the potential for impacts to corals from oil, and the

LeGore et al. studies suggest an enhancement of impact with the use of

chemical dispersants.

ACUTE EFFECTS

Contrary to some earlier research findings and review conclusions,

exposure to oil and oil spills has been shown to cause acute oil

toxicity. Some studies have involved somewhat extreme exposure

scenarios, but other, more realistic experiments have

demonstrated relatively rapid toxic impact. Other studies have

shown that a brief exposure may not result in immediate death, but

does so after an extended period of time.

A review of laboratory and field studies on acute effects of oil to corals can be

confusing. Widespread coral mortalities following actual spills have been

reported only infrequently, even when (as reported by Ray 1980) associated

reef dwelling organisms have perished. Fucik et al. (1984) suggested that

acute toxicity impacts were probably not a good indicator of oil effect, and

stated it is more likely that adverse effects to the coral would be manifested

in sublethal forms.

There were no reported mortalities of corals after the unprecedented Gulf

War spill. As previously detailed in the summaries of larger-scale

experiments, the 1984 TROPICS experiment in Panama (Ballou et al. 1987;

Dodge et al. 1995) showed no short- (0-20 months) or long-term (10 years

later) effect to corals in an intentionally oiled zone. LeGore et al. (1989)

found a similar lack of effect in their field experiment.

Shinn (1989), arguing that oil is not among the biggest threats to coral survival,

related results of a simple qualitative experiment he performed. He placed
24

pieces of staghorn and star corals in plastic bags of Louisiana crude oil and

seawater and left them exposed for 90 minutes before returning them to

clean seawater. Shinn said that corals appeared normal the next day, as well

as fourteen days later. He attributed this apparent lack of effect (and that

from a subsequent half-hour immersion in pure Louisiana crude) to the

protective qualities of mucus.

However, there are many notable exceptions to a conclusion of little

apparent acute oil toxicity in corals. These include the previously mentioned

1986 Bahía Las Minas spill in Panama, whose effects were extensively

documented. In that incident, researchers found widespread coral mortality

attributed to the spill, as will be detailed below.

Results from laboratory experiments investigating acute toxicity of oil to

corals are somewhat equivocal, and have shown a range of impacts. While it

is not possible (nor is it our intent) to reconcile the apparent contradictions,

some of the variation may derive from differences in exposure methods.

That is, laboratory studies on acute toxicity of oil have involved several

different means of exposing test corals to oil. These have included complete

immersion in refined and crude products, coating with oil, and mixing oil into

water and using only the water for experiments. In an actual spill, reef corals

would be expected to be directly exposed to oil infrequently, if not rarely.

Nevertheless, the more direct (one might say extreme) exposures provide a

useful endpoint for understanding the acute toxicity of the tested oils on the

tested corals.

Elgershuizen and deKruijf (1976) examined the acute toxicity of four crude

oils (Nigerian, Forcados, Tia Juana Pesado, and Forcados long residue) to the

hermatypic coral Madracis mirabilis. Oil and water test solutions were

prepared in two ways: water soluble fraction (WSF) of oil floating on

seawater, in which a known quantity of oil was floated on the surface of

seawater for 24 hrs before it was removed and the remaining seawater used

for dilutions; and as an oil-seawater mixture, in which a known quantity of oil

was added to seawater and stirred for 24 hrs (dispersant/seawater and

oil/dispersant/seawater mixtures were also tested; those results may be

found in the original reference). Toxicity endpoints for the experiment were

RD50 and LD50, with those terms being defined somewhat unconventionally in

this study: RD50 concentrations were the 50 percent response doses after

the 24 hr test period; LD50 concentrations were the 50 percent mortality

doses after an additional 24 hrs of recovery in running seawater.

Nearly all M. mirabilis colonies exposed to solutions derived from oil on the

surface recovered, and thus no mortality curve could be generated. Recovery

was also quite high for solutions of Nigerian and Forcados crudes mixed with

seawater. Elgershuizen and deKruijf found that oils mixed with seawater

were more toxic than solutions from oils floated on the surface. Test
25

solutions from Forcados long residue and Tia Juana crude were more toxic,

but lower concentrations did not induce permanent damage. It is, however,

unclear how the authors defined “permanent” within the context of this

experiment.

Elgershuizen and deKruijf concluded that the oils alone were of low acute

toxicity to coral colonies. In this case, the authors were much more

concerned about the toxic impacts of chemical dispersants, alone and in

combination with oils.

Johannes et al. (1972) conducted oil exposure experiments on 22 species of

coral at Eniwetok Atoll. Because the upper portions of coral reefs in the

Pacific region are sometimes exposed during low spring tides, the

researchers were interested in studying how oil affected the corals under

these conditions. Two specimens of each of the coral species were floated in

frames with a portion of each exposed to the air and the remainder

submerged. Santa Maria crude oil was then poured into the water around

one frame containing the corals, but not directly on them (the other frame

was left as a control). Natural wave action coated the exposed surfaces with

oil. Exposed corals were left in the frame for about 1.5 hrs, at which point all

specimens were placed in clean water. They were then observed over the

next four weeks.

Branching corals, such as those in the genera Acropora (the most abundant

genus in the Indo-Pacific region) and Pocillopora, were most susceptible to oil

coating and retention. Corals such as Fungia sp. and Symphyllia sp., which are

characterized by large fleshy polyps and abundant mucus, retained almost no

oil after immersion for a day and showed no subsequent damage. Members

of the genera Turbinaria, Favia, Plesiastrea, Favites, Psammocora, Astreopora,

Symphyllia, Montipora, and Porites showed intermediate oil affinities. In

locations on the colonies where oil adhered in patches greater than a few mm

in size, “complete breakdown” of tissue occurred. Areas where oil did not

adhere appeared healthy. Control colonies remained healthy throughout.

It seems clear from this study that direct contact with crude oil kills coral

when the oil adheres. This contrasts with the several other studies that

indicated that proximity of submerged corals to surface oil generally resulted

in few discernible acute impacts. For example, Johannes (1975) described

unpublished experiments in which he and others floated five types of oil over

groups of the Hawaiian corals Porites compressa, Montipora verrucosa, and

Fungia scutaria for 2.5 hrs. No visible evidence of injury was found over 25

subsequent days of observation.

The observation by Johannes et al. that branching corals were more

susceptible to oil exposure is consistent with the findings of others who have

made field studies in oil affected areas. Guzmán et al. (1991, 1994) noted that

in the Bahía Las Minas spill, nearly all branching corals were killed and thus,
26

longer-term studies could be performed only on massive species of coral.

Similarly, Hudson et al. (1982) found that, in areas around oil production

wellheads, massive species like Porites lutea preferentially survived over

branching genera like Pocillopora or Acropora. The latter showed an estimated

70-90 percent reduction.

The differential susceptibility to oil seems to be more closely linked to

physical form than taxonomy. This distinction can be confusing, since the

literature (e.g., Dodge et al.1995; LeGore et al.1989) describes field evidence

supporting the notion of increased tolerance to oil for some species of

Acropora—the same taxon described as being less tolerant above. This may be

explained by the fact that species of Acropora assume many forms, from

massive to arborescent (branching). Moreover, colonies within the same

species can assume different forms, depending on environmental or biological

conditions (Veron 1986).

In a sparsely described scoping experiment, Grant (1970) placed two of each

specimen of Favia speciosa in three 15-gallon aquaria. In two of the tanks, he

floated about three pints of Moonie crude oil, and in one of these he varied

the water level daily to simulate tidal change. In this way, oil was permitted to

contact the corals for about five minutes over five days. At the end of eight

days, oil was removed from the two exposed aquaria. The corals were

maintained in tanks for another 16 days and Grant related that all were alive

and “apparently unaffected.” It is worth noting that he qualified the results

heavily and concluded, “The experiment described above cannot be regarded

as definitive: it is indicative only, and calls attention to a need for substantially

expanded inquiries...”

Cohen et al. (1977) studied the effect of Iranian (Agha Jari) crude oil on

colonies of the Red Sea octocoral Heteroxenia fuscescens under both static and

continuous flow assay conditions. For static tests, coral colonies were placed

in 3 L of aerated seawater and oil was introduced at nominal concentrations

of 1, 3, 10, and 30 ml/L (oil was simply added to the water surface at the

various calculated concentrations after a 3-hr acclimation period). Exposure

time was 96 hrs. LC0, LC50, and LC100 concentrations were then calculated.

Flow-through assays were also conducted in 1500-L fiberglass tanks. The

highest oil concentration used was 10 ml/L, added as a single dose on the

surface of the water. The exposure period was 168 hrs.

Table 1 summarizes acute lethality results from both experimental setups.

The 96-hr. LC50 concentration was determined to be 12 ml/L. The results

reflect the fact that differences in experimental exposure (static or flowthrough) do affect toxicity. This becomes more evident at longer exposure

times, with lower toxicity results in the flow-through setup.
27

Table 1. Concentrations of Iranian crude oil in ml/L added to medium at

start, fatal to 0, 50, and 100 percent of Heteroxenia colonies under

static and continuous flow conditions, from Cohen et al. (1977).

Static

Continuous

 24 hr. 48 hr. 72 hr. 92 hr. 168 hr. 

LC0 30 3 1 1 10

LC50 >30 >30 17 12 >10

LC100 >30 >30 >30 30 >10

Although the results suggest a relatively low overall toxicity of crude oil to

Heteroxenia fuscescens, the previously discussed consideration of nominal

rather than measured exposure concentrations should be mentioned again:

the water column concentration resulting from the specified nominal

concentrations of oil simply added to water would be much lower than those

listed.

Reporting an actually measured concentration would result in a much higher

toxicity result. As a consequence, interpreting and applying the findings to

situations that might be encountered during a spill is quite difficult. Because of

the uncertainties inherent with nominal exposure concentrations, the

apparent differences with time and with the nature of experimental exposure

(static or continuous) are more interesting. Cohen et al. showed that toxicity

of a given concentration of oil increased with longer time of exposure, and

that continuous flow conditions result in lower toxicity values relative to

static.

One conclusion we can draw from this study is that experimental setup type

can affect toxicity results. In a broad analysis of aquatic toxicity, Mayer and

Ellersieck (1986) compared 123 paired static and flow-through toxicity results

and found that for the group of chemicals they studied, static test most often

(53 percent) resulted in lower acute toxicity than flow-through tests. The

flow-through was less toxic in only 10 percent of the pairs. . Mayer and

Ellersieck suggested that degradation or hydrolysis products of the given

contaminant that accumulated in static test vessels might have been an

influence in the latter cases; this might be the case for petroleum

hydrocarbons and corals. Cohen et al. themselves attributed the lower

toxicity in flow-through exposures to “...the continuous removal (of oil) in

the medium and probably to a reduced biomass per unit volume in tanks as

compared to jars.”

Birkeland et al. (1976) performed a series of three experiments with

hermatypic corals from the eastern Pacific and from the Caribbean. Results

were also reported in Reimer (1975). Coral species used were Pocillopora cf.

damicornis, Pavona gigantea, Psammocora stellata, and Porites furcata. These

experiments involved some of the most extreme oil exposure scenarios
28

encountered in our review. While it seems unlikely that natural reef corals

would experience these kinds of exposures in an actual spill, the results help

to establish one end of the range of acute effects.

In their first experiment, two colonies of Pocillopora cf. damicornis were

completely submerged in marine diesel oil for 30 minutes. The corals were

then rinsed thoroughly and placed in an aquarium. Control colonies were

similarly treated, with seawater substituted for the marine diesel.

Results: The exposed colonies initially survived a 30-minute exposure to

pure marine diesel, despite tissue rupture especially at the edges of the

colonies. After 17 days, however, 70 percent of the polyps were dead and

those still living had mouths open and mesenterial filaments extended

(controls showed none of these responses and lived for 35 days without

significant tissue death). The authors noted a “massive” initial extrusion

of zooxanthellae.

In the second study, two colonies of P. cf. damicornis were placed in marine

diesel, three in Bunker C oil, and three in seawater, for exposure periods of

1 minute. Branches and small colonies of Pavona, Psammocora, and Porites

were also subjected to similar experimental conditions to evaluate species

differences.

Results: All the colonies had similar degrees of tissue death for the first

week; but after 13 days obvious differences between oiled and unoiled P.

cf. damicornis were noted. For example, within 13 days colonies exposed

to marine diesel lost nearly all living tissue and those exposed to Bunker

C lost 70-84 percent. After 16 days, both oil-exposed groups had lost

nearly all living tissue. In contrast, control colonies sustained over 95

percent.

In the third experiment, an individual branch on a given colony was exposed to

diesel, Bunker C, or seawater, for 30 seconds. Another branch on the same

colony was left untouched.

In all cases, oil was removed from experimental colonies by submerging them

in seawater and removing the resulting surface film with an absorbent tissue.

They were then rinsed in running seawater for 30 minutes.

Results: Somewhat equivocal, few differences over a 1-month period;

some sharper differences appeared after 71 days, but no trends were

evident that could be related to treatments. After 109 days, all colonies

treated with Bunker C as well as one control were dead; the remaining

controls and the marine diesel colonies had low cover of living tissue.

Several colonies showed extensive bleaching within 5-13 days after the

experiment commenced, but all but one had recovered by day 27.
29

Reimer (1975) reported a fourth experiment in this series, one in which

colonies of the four species were exposed to 1-4 ml marine diesel added to

the surface of 50 ml or 250 ml finger bowls, for periods of either 30 minutes

or 4 hrs.

Results: Oil on the surface of the water caused synchronized contractions

in P. cf. damicornis colonies, along with mouth opening. When corals were

exposed for 4 hrs, 32 to 50 percent of the colonies died over a 93-hr.

post-exposure period. For the other three species, a similar mouthopening response was observed after exposure. This reaction was

transient, with duration after return to clean seawater lasting from 15

minutes in Pavona to 4 days in Porites.

Rinkevich and Loya (1977) have performed a number of studies with Red Sea

corals, especially Stylophora pistillata. Although most have examined chronic

or longer-term consequences of oil exposure, they also reported on the

acute effects of water-soluble fractions of Iranian crude oil on coral planulae.

The test mixture was prepared by mixing 1 part crude oil with 99 parts

seawater, with the resulting aqueous solution considered as 10 ml/L (the

authors acknowledged that only a minor portion of the oil would have actually

dissolved in the seawater).

At 144 hours, none of the planulae had died in the control exposure, while

more than 50 percent had died in the 1, 5, and 10-ml crude oil/L seawater

aqueous fractions.

Rinkevich and Loya also tracked S. pistillata colony mortality rates in the field,

at a chronically polluted reef near the oil terminals of Eilat, and at an unoiled

reference reef 5 km to the south. They checked 59 healthy colonies in the

polluted area and 39 in the control area for viability every four months. After

one year, 42.3 percent of the oiled area colonies had died, compared to 10.3

percent of the controls. This represented a significant (p < 0.01) difference in

mortality.

There was no mention in the referenced article of exposure documentation,

which would significantly bolster the inferred link between chronic oil

contamination and coral viability.

Te (1991) studied the toxicity of gasoline, motor oil, and benzene to Hawaiian

reef coral planulae (Pocillopora damicornis). Te performed open- and closedsystem (i.e., sealed to limit volatilization) bioassays with gasoline:oil mixtures

and with benzene. For the gas:oil mixture exposures, three replicates each of

15 planulae were exposed to nominal concentrations of: 5, 10, 50, and 100

ppm mixtures of gasoline and motor oil in 50 ml petri dishes (open system);

and 1, 5, 20, and 100 ppm in 200 ml sealed bottles (closed system). Hourly

observations were made for the first 6 hrs, 6-hr intervals for three days, and
30

12-hr. intervals for the final 13 days. For benzene studies, a closed system

setup as detailed for gasoline was established.

Te did not document any mortality from gasoline:oil mixtures in the open

system experiments, although total mortality occurred with the 100-ppm

concentration in the closed system. No mortality was observed in the

benzene exposures. Te concluded that in contrast to many organisms that

readily showed mortality at even very low concentrations, P. damicornis

planulae seemed to be resistant to oil exposure.

A field study of the Bahía Las Minas oil spill in Panama (Jackson et al. 1989)

reported an extensive mortality of both intertidal reef flat corals (Porites spp.)

and subtidal reef corals (Diploria clivosa, Porites astreoides, and Siderastrea

siderea) that was attributed to the spill. S. siderea was found to have been

particularly vulnerable, with new partial mortality disproportionately

common on heavily oiled reefs one year after the spill. Burns and Knap

(1989) commented that these findings of acute impact from a spill stand in

sharp contrast to the conclusions from laboratory dosing experiments and

small-scale field studies suggesting only transient effects.

A longer-term summary of impacts in Bahía Las Minas can be found in

Guzmán et al. (1994). They assessed acute (recent mortality) as well as

sublethal (growth) impacts to the species listed above. At heavily oiled reefs,

percentages of recently injured (as identified by bare white or lightly

overgrown skeleton exposure) corals were higher for all three species.

However, there were peaks immediately after the spill and also during

another period spanning 3-5 years post-spill. The latter impacts were

attributed by Guzmán et al. to be linked to a series of diesel fuel spills at the

electrical generation plant in Bahía Las Minas.

This comment by Guzmán et al. suggests one of the major difficulties in trying

to isolate impacts attributable to a specific spill incident from other possible

sources of impact: the fact that a myriad of other natural and human-induced

influences can affect a community. This is the downside to the real-world

example embodied in an actual spill.

Harrison et al. (1990) describes a set of experiments performed in Australia

using a Great Barrier Reef coral species (Acropora formosa) . This laboratory

study is particularly interesting because it showed both acute and chronic

toxicity impacts from oil in the water (water-accommodated fraction, WAF)

at measured concentrations which might be encountered during a spill.

Branches of A. formosa tolerated 6-hr. exposures to 5-10 ppm (measured in

the water) marine fuel oil, but with 12 to 24 hr. exposure to the same

concentrations, the colonies became stressed (increased mucus production,

expelled zooxanthellae) and died. After 48 hrs, virtually all of the tissue in the

5 and 10-ppm treatments had disintegrated. The chronic and potential

indirect toxicity results will be discussed in subsequent sections.
31

Gardiner and Word (1997) and Gardiner et al. (1998) also documented acute

and chronic toxicity effects in a branching coral (Acropora elsyii) exposed to

water-accommodated fractions (WAFs) of fresh and artificiallyweathered

Campbell condensate and Stag crude oil. Artificial weathering consisted of a

distillation process in which the source oil products were heated to drive off

the more volatile fractions and simulate the changes that occur to oil in the

environment. The water-accommodated fractions were prepared using

modifications to a standard protocol developed by Environment Canada

(Blenkinsopp et al., 1996), and the 100 percent WAF concentrations of total

petroleum hydrocarbons were estimated to fall between 2 mg/L and 20 mg/L.

Table 2 shows (concentrations of the 100 percent WAFs measured by

infrared spectrophotometry. For toxicity tests, 100, 50, 10, and 0 percent

concentrations of the stock WAF mixture were used.

Table 2. Measured (by infrared spectrophotometry) replicate

concentrations of 100-percent solutions of water-accommodated

fractions of test oils used in coral toxicity experiments.

Concentrations in μg/L (ppb). From Gardiner and Word (1997).

Oil/Treatment Concentrations (ppb)

Fresh Stag...........................................................219...................273

Stag/200°C..........................................................138...................140

Stag/250°C..........................................................83.....................102

Fresh Campbell................................................7900................540

Campbell/150°C...............................................3430................949

Campbell/200°C...............................................638...................126

Table 2 shows a generally consistent trend of decreasing solubility and/or

accommodation of hydrocarbons into the water with increased weathering.

This makes intuitive sense, since the more volatile fractions lost during

weathering are also the more soluble. The table also shows the distinct

differences in solubility characteristics with different oil products (condensate

and crude). Finally, the replicate measurements for the Campbell condensate

in particular illustrate the great variability that can occur in the preparation of

nominally identical mixtures.

Gardiner and Word (1997) did not elicit an acute toxicity response in 144-hr

tests except for the fresh Campbell condensate at 100 percent strength.

Coral fragments exposed to the full-strength fresh Campbell WAF

experienced 100 percent mortality, which occurred in the first hours of

exposure. Sublethal exposure experiments are discussed below in the

chronic toxicity section.

A petroleum product that is attracting an increasing amount of interest from

power generating entities worldwide is a material known primarily by its

trade name, Orimulsion. Orimulsion is a natural bitumen in a freshwater

emulsion, stabilized by the addition of non-ionic surfactants. The bitumen is
32

designated as Cerro Negro and is produced in the Orinoco Belt in eastern

Venezuela. It is being marketed as a cheaper alternative fuel for power

generation, but environmental concerns have complicated its ready acceptance

and approval in some countries (e.g., the U.S.).

Brey et al. (1995) reported on toxicity evaluations they conducted for

Orimulsion and its major constituents, and for No. 6 fuel oil. Among the

tests performed were acute toxicity studies using the coral Tubastrea aurea.

The methods for these tests were not described in great detail. It appears

that exposure concentrations for petroleum products were measured, but

only as a gross analysis of oil and grease. In the case of the No. 6 fuel oil

solutions, the stock mixture was held under refrigeration for one week

before tests were performed.

Acute toxicity results (96-hr. LC50) in Tubastrea aurea were reported to be

112 mg/L (ppm) for Orimulsion; values for bitumen and No. 6 fuel oil were

not calculated “because no mortality was observed at the highest

concentrations used” (25.8 and 43.97 mg/L, respectively).

Although Brey et al. commented that T. aurea seemed to be more sensitive to

Orimulsion than to the other petroleum products, the uncertainties related

to methodologies suggest cautious interpretation of these results. It is

unclear whether concentrations used for calculating LC50 values were nominal

or measured. Water-accommodated fractions were apparently chemically

analyzed using a gross oil and grease methodology. Moreover, stock

solutions, especially that for the No. 6 fuel oil, were not prepared in a

conventional way (i.e., held under refrigeration for an extended period).

These considerations complicate interpretation of the results within the

study and severely limit comparison to other toxicity results.

CHRONIC EFFECTS

Chronic effects of oil exposure have been consistently noted in

corals and can be substantial, ultimately killing the colony. A

number of chronic impacts have been described, including

histological, biochemical, behavioral, reproductive, and

developmental effects. Cumulative impacts resulting in mortality

are also suggested. Field studies of chronically polluted areas and

manipulative studies in which corals are artificially exposed to oil

also suggest that some coral species are more resistant to the

detrimental effects of oil than other species.

It may be stating the obvious that oil spills can take many forms, and that a

catastrophic release of oil such as a spill or blowout may also result in

chronic, or long-term sublethal impacts to an area. In addition, chronic effects

to sensitive resources like coral reefs may also occur without an identifiable
33

incident, i.e., via non-point source contamination. In either case, ample

research evidence demonstrates that oil can cause a number of sublethal but

serious impacts to coral. It is a fairly robust literature, and is characterized by

a qualitatively broad range of impact.

Coral researchers such as Guzmán et al. (1994) have suggested that oiled

corals perform a tradeoff between functions related to exposure response

(e.g., cleaning and damaged tissue regeneration) and normal energy

expenditures (e.g., growth and reproduction). The literature on chronic and

sublethal effects of oil on corals supports this, and the resulting studies focus

on the questions of whether oil increases the stress responses or decreases

normal physiological functions. It is reasonable to presume that the

reallocation of energy in the face of stress imposed by a spill would ultimately

reduce the fitness of the affected corals, as would be expected for any

organism responding to any stress.

Field studies examining chronic effects are less common than laboratory

experiments because of the length of time necessary to study longer-term

effects of oil exposure to corals, the lack of control over environmental

conditions that may influence results, and the generally more subtle

measurements necessary to document a sublethal impact. . Those field

efforts that do take into account longer-term effects often rely on gross or

more integrative measures of health, such as areal cover or simple presence

and absence. An example of such a study is described by Bak (1987), who

compared coral reef status in a chronically contaminated embayment on the

island of Aruba in the southern Caribbean Sea. Between 1929 and 1985, a

large oil refinery (heavy Venezuelan crude) operated in this location with, as

listed by Bak, “...all accompanying sources of pollution such as spills, refinery

waste water discharge and eventually cleanups with dispersants (Corexit).” A

continuing chronic source of contamination—a sheen at the harbor

entrance—was noted a year after the refinery was closed.

Bak surveyed 24 species of coral in the study, and concluded that there

appeared to be a clear relation among the condition of the reef structure and

the coral communities, the location of the oil refinery, and the current

pattern. That is, the major deterioration of the reef occurred in front of the

refinery and immediately downcurrent. Coral species such as Montastrea

annularis and Agaricia agaricites were absent in these areas but became

abundant upstream of the facility. In contrast, Diploria strigosa showed a

completely opposite distribution, suggesting an increased tolerance to oil (the

possibility that D. strigosa is more resistant to oil exposure was supported by

the laboratory studies of Dodge et al. 1985).

Some reviewers have asked how well laboratory studies of chronic effects

relate to actual field conditions. That is, do the artificial strictures of the

laboratory unrealistically skew results so that they have minimal relevance to
34

a real spill scenario? As we have noted, field and laboratory studies of oil

toxicity to corals often yield conflicting or confounding results. In an effort to

address this, Rinkevich and Loya studied the impacts of chronic exposure to

oil in the field (1977) and then compared these results to those obtained in

long-term laboratory exposures (1979). Loya, Rinkevich, and their colleagues

have researched oil effects to Red Sea corals (the branched hermatypic coral,

Stylophora pistillata in particular) for the last 20 years. They have used a

number of sublethal responses as endpoints for their studies and, at least for

S. pistillata, have generated a substantial body of information for chronic

impacts of oil exposure. Rinkevich and Loya obtained results that were

consistent with both the field and laboratory conclusions, which provides at

least one set of experiments suggests the relevance of laboratory results to

field situations.

An interesting approach to combining the most desirable aspects of lab

experiments (e.g., controlled exposure conditions) with those of the field

(realistic environmental conditions) was that of Dodge et al. (1984) in which

corals were exposed to oil in the laboratory but then moved to a field setting

for subsequent long-term observation (around a year). Their results will be

discussed later.

We reviewed many studies of chronic effects of oil exposure to corals. A

number of studies used multiple endpoints for exposure impact, and it

became apparent that we would need to organize or group the results in

some fashion for summary and synthesis. Fucik et al. (1984) created a list of

laboratory studies documenting sublethal oil impacts. Their table, updated to

include additional endpoints and more recent studies, is reproduced below as

Table 3.

The table is instructive in that it shows the broad range of impacts from oil

exposure that researchers have identified; it also links the researchers with

endpoints and serves as a quick reference if a reader has an interest in a

specific kind of effects endpoint. The list here, however, is not necessarily

comprehensive with respect to studies reviewed for this report.

We have chosen to group the reported endpoints into the following

categories: behavioral, fecundity and reproduction, larval; histological,

calcification and growth, surface cover, photosynthesis, and mucus and lipids.

This list is also not a comprehensive one, but it seems to encompass most of

the reported effects in the literature. Any that did not fit into the eight

categories will be discussed separately.

Behavioral Endpoints

Lewis (1971) exposed four species (Porites porites, Agaricia agaricites, Favia

fragum, and Madracis asperula) collected on the west coast of Barbados to an

unspecified crude oil by soaking strips of filter paper in the petroleum and
35

then submerging them near but not in physical contact with test corals. The

exposure period was 24 hrs. Lewis used three behavioral endpoints as effects

indicators: tentacle extension, feeding, tentacle retraction upon stimulus

(“tactile,” in table below), and development of ruptures in the oral disks

through which septal filaments were extruded (“septal filaments absent,” in

table). The results of the oil exposures are summarized below in Table 4.
36

Table 3. Stress responses shown by corals exposed to oil and oil fractions

(adapted from Fucik et al. 1984).

Response References

Tissue death Johannes et al. (1972); Reimer (1975);

Neff and Anderson (1981); Wyers et al.

(1986)

Impaired feeding response Reimer (1975); Lewis (1971); Wyers et

al. (1986)

Impaired polyp retraction Cohen et al. (1977); Elgershuizen and de

Kruijf (1976); Neff and Anderson (1981);

Knap et al. (1983); Wyers et al. (1986)

Impaired sediment clearance ability Bak and Elgershuizen (1976)

Increased mucus production Mitchell and Chet (1975); Peters et al.

(1981); Wyers et al. (1986); Harrison et

al. (1990)

Change in calcification rate Birkelund et al. (1976); Neff and

Anderson (1981); Dodge et al. (1984);

Guzmán et al. (1991, 1994)

Decreased growth (wet-weight biomass) rate Gardiner and Word (1997)

Gonad damage Rinkevich and Loya (1979b); Peters et al.

(1981)

Impaired fertilization Negri and Heyward (2000)

Premature extrusion of planulae Loya and Rinkevich (1979); Cohen et al.

(1977)

Larval death Rinkevich and Loya (1977)

Impaired larval settlement Rinkevich and Loya (1977); Te (1991);

Kushmaro et al. (1996); Epstein et al.

(2000); Negri and Heyward (2000)

Coenosarc tissue damage Peters et al. (1981)

Expulsion of zooxanthellae Birkelund et al. (1976); Neff and

Anderson (1981); Peters et al. (1981)

Decrease in chlorophyll a Gardiner and Word (1997)

Change in zooxanthellae primary production Neff and Anderson (1981); Cook and

Knap (1983); Rinkevich and Loya (1983)

Muscle atrophy Peters et al. (1981)
37

Table 4. Range of oil concentrations (ppm, nominal) at which impairment in

specified parameter was noted in 50 percent of test colonies, by

species (Lewis 1971).

TENTACLE EXTENSION

Porites porites Madracis asperula Favia fragum Agaricia

agaricites

100-200 ppm 10-50 ppm 10-50 ppm 200-500 ppm

FEEDING

Porites porites Madracis asperula

100-200 ppm 10 ppm

TACTILE

Porites porites Madracis asperula

>1000 ppm 10-50 ppm

SEPTAL FILAMENTS ABSENT

Favia fragum Agaricia

agaricites

500-1000 ppm >1000 ppm

From our current perspective, the major shortcoming of this study stems

from the use of nominal oil exposure concentrations only. The nominal oil

concentrations make it difficult to compare or extrapolate these results to

other situations. If we assume an internal consistency in the way the corals

were exposed to oil (perhaps a big assumption) then patterns across species

emerge: Madracis asperula was the most sensitive to oil exposure, and

Agaricia agaricites least sensitive. The other two species were of intermediate

susceptibility. Lewis suggested that branching forms such as Porites and

Madracis were more affected by exposure than the other two encrusting

species. Johannes (1972) also noted this link between form and susceptibility

for acute effects. (Lewis also examined the toxic effects of exposure to an oil

dispersant but those results are not presented here).

The problem in assuming that oil exposure was consistent with consistency in

methodology is that others have made the comparison (see Table 2) and

shown that actual exposures presumed to be equal can vary considerably,

over an order of magnitude. Experiments relying on nominal oil

concentrations have to be interpreted with great caution.

In addition to acute lethality, Cohen et al. (1977) used simple behavioral

endpoints in determining effects of Iranian crude oil to Heteroxenia fuscescens.

As described in the preceding section on acute toxicity experiments, the

researchers used both static and flow-through setups to assess effects of

exposure to Iranian crude oil at four nominal concentrations (1, 3, 10, and 30

ml/L). They used two behaviors—abnormal pulsation and abnormal response

to mechanical stimulation—and found that oil-exposed colonies showed a

reduced pulsation rate and an uncoordinated response to stimulation.
38

Cohen et al. concluded that, while their exposures did not result in

substantial acute toxicity, they also suggested that sublethal exposures could

produce latent adverse effects that would not be reflected in short-term

assays.

Wyers et al. (1986), Knap et al. (1983), and Cook and Knap (1983) were

companion studies designed to examine toxicity of chemically dispersed oil to

the brain coral, Diploria strigosa. As a part of these studies, the effects of

physically dispersed oil (i.e., no chemical dispersant) were also assessed. The

experimental design was intended to inject a degree of spill realism into coral

and oil studies, by using a flow-through system that mixed Arabian Light crude

oil with water (also with dispersants as well). D. strigosa colonies were

exposed for a 24-hr. period. Wyers et al. performed an initial study,

presumably for scoping purposes, targeting 1,5, and 20 ppm total oil

concentration; because most of the colonies exposed at 1-5 ppm appeared

unaffected, subsequent experiments (including those of Knap et al.) used 20

ppm as their targeted exposure concentration. As illustrated in Figure 2,

measured concentrations (hexane extracts by fluorescence spectrometry)

showed a fair amount of variability but were close to the desired level.

0 2 4 6 8 10 12 14 16 18 20 22 24

20

40

60

0

Oil Concentration (mg/L)

Time (hrs)

Figure 2. Fluctuations of oil concentrations measured by fluorescence

spectrometry during 24-hr dosing for physically dispersed oil;

nominal concentrations were 20 ppm. From Knap et al. (1983).

Wyers et al. used tentacle extension as the response measure for exposure,

along with other parameters such as the presence of adherent mucus/oil,

mesenterial filament extrusion, loss of pigmentation, and tissue swelling.

They showed that while exposure to 20-ppm oil in the water column induced

stress-related symptoms, normal appearance was usually resumed within 2

hrs to 4 days following the 24-hr exposure period. They concluded that the

observed effects were unlikely to impair overall coral viability. Wyers et al.

did indicate that tissue rupture and associated lesions could be an exception

due to the possibility of increased infection or predation. However, these
39

lesions were found only after exposure to the highest tested concentration,

20 ppm, and not with 1-5 ppm.

Knap et al. continued the work of Wyers et al. and found that the oil-exposed

corals were characterized by a decline in tentacle expansion. One week after

the 24-hr exposure, expansion behavior typical of the controls was recorded.

No longer-term differences in skeletal growth were observed with

treatment, although the authors noted that high intercolony variability made

differentiation of potential subtle impacts difficult.

Bak and Elgershuizen (1976) studied the abilities and patterns of 19 species of

hermatypic corals to reject, or cleanse themselves, of oiled sediment. The

oiled sediment results were referenced against patterns for clean sediment.

Corals were collected from the fringing reefs of the southwest coast of

Curaçao. The oils used were four of the same oils employed by Elgershuizen

and deKruijf (1976)—Nigerian, Forcados, Tia Juana Pesado, and Forcados long

residue—with the addition of Lagomar short residue.

Bak and Elgershuizen could find no evidence of oil adsorption to coral tissues,

and no sign of active ingestion of oil droplets. Oil introduced into and onto

the corals was actively cleared by the colonies. If the species was a mucus

secretor, oil could be incorporated into mucus for up to 5 hrs. There was no

difference in clearance rates or patterns between oiled sediment and clean

sediment.

Fecundity and Reproduction 

In a laboratory experiment, Rinkevich and Loya (1979) split S. pistillata

colonies, with one portion being held as a control and the other exposed to

oil. The exposed colonies were held in tanks and Iranian crude oil was

introduced on the surface of the water once each week over periods of two

and six months. While oil did not contact the colonies directly, they were

exposed to the water-soluble fraction of the crude floated on the water’s

surface.

The researchers found that after two months, 75 percent of the exposed S.

pistillata colonies showed a significant decline in the number female gonads

per polyp. After six months, Rinkevich and Loya documented a significantly

higher mortality among exposed colonies than in the controls (no mortality

had been noted after two months). They suggested that this reflects a latent

cumulative effect of chronic oil exposure.

The same researchers (Rinkevich and Loya, 1977) performed field studies of

the effect of chronic oil contamination on S. pistillata colonies. They noted a

significant difference in the number of colonies with gonads in polyps between

an unoiled reference area and a reef located near oil terminals in the northern

Gulf of Eilat (Red Sea). One hundred three mature colonies from the oil port
40

area and 98 from the control reef were studied. About 75.5 percent of

control colonies contained gonads in polyps, compared to 44.6 percent in the

oil terminal colonies.

Guzmán and Holst (1993) studied the major reef-building coral species,

Siderastrea siderea, in the Bahía Las Minas (Panama) area, focusing on potential

reproductive impacts from chronic oil exposure. They measured coral

fecundity, as reflected by the number of gonads per polyp and gonad size, in

heavily oiled and unoiled reefs. The study took place 39 months after the

major 1986 spill, summarized earlier in the case studies section.

Guzmán and Holst found no difference between oiled and unoiled areas in the

number of coral colonies with gonads at any stage of development and also in

the number of gonads per colony. However, gonad size did vary significantly

with oiling, with larger gonads occurring at unoiled reefs. The authors

suggested this reflected a stress-induced lowering of fecundity at the oiled

sites, and that gonad size might be used as a sensitive indicator of coral

viability.

In a more direct look at the effects of oil on critical reproductive processes in

corals, Negri and Heyward (2000) performed a series of studies to determine

the effect of water-accommodated fractions of a heavy Australian crude oil

(Wandoo) on fertilization success for the broadcast spawning coral, Acropora

millepora (they also tested WAFs from production formation waters, chemical

dispersant mixed with the crude, and neat dispersant). Egg and sperm were

isolated from Great Barrier Reef colonies and used for the fertilization

assays. The test mixtures of egg, sperm, contaminant WAF, and filtered

seawater were held for 4 hrs before termination and preservation.

Negri and Heyward estimated the total hydrocarbon concentration in their

stock crude oil WAF mixture (100 percent) to be 1.65 ppm by means of UV

fluorescence. In the absence of dispersant, the WAF of crude oil alone failed

to inhibit fertilization up to a concentration of 0.165 ppm total hydrocarbon,

or a ten- percent dilution of the stock solution. Dispersant alone was less

toxic (significant fertilization inhibition at 10 ppm), but one and ten percent

mixtures of dispersant and crude oil were more toxic (inhibition at 0.225 and

0.0325 ppm, respectively). Dispersed crude oil completely inhibited

fertilization at 0.325 ppm, equivalent to a 1- percent dilution of crudedispersed stock mixture.

Effects to Larvae and Larval Development 

Rinkevich and Loya (1977) documented the numbers of planulae released

from S. pistillata colonies in chronically oiled and control reefs. The two areas

were defined by proximity to an oil port facility, and apparently no chemical

measurements were made of exposure conditions. They performed this

study by enclosing 35 large colonies in each area with plankton nets, and found
41

that most (68.6 percent) in the control reef released more than five planulae

per coral head, while most in the contaminated reef (85.7 percent) released

less than five. Rinkevich and Loya concluded that coral fecundity in the control

reef was four times greater than in the chronically contaminated area (this

was based on the total number of planulae collected at the two colony groups,

181 in oiled vs. 772 in control).

The authors also studied the settlement and viability of planulae in the two

areas, and found that colonization onto artificial settlement plates was

significantly higher in control reef areas.

In another series of experiments, Loya and Rinkevich (1979) exposed S.

pistillata colonies to water-soluble fractions (WSFs) of Iranian crude oil (1:100

stock mix). Actual concentration of oil in the water was not determined.

They found that the crude oil WSF induced the coral to prematurely expel

larvae into the water, and additionally large numbers of symbiotic

zooxanthellae were also shed (in the absence of disturbance, S. pistillata

usually sheds larvae only at night). The authors also observed abnormal

movement in the larvae, even at the lowest dilution exposure. Loya and

Rinkevich suggested that the incompletely developed planulae released by the

stressed corals would have a low probability of survival.

In their experiments with Heteroxenia fuscescens, using Iranian crude oil,

Cohen et al. (1977) found that exposure to the oil resulted in greater

numbers of larvae expelled relative to unoiled controls. Actual numbers

were not reported, although the differences in numbers of larvae were

noticed after 72 hrs exposure and appeared to diminish after 96 hrs of

recovery in clean water.

Rinkevich and Loya (1977) exposed planulae of S. pistillata to WSF of Iranian

crude oil (concentrations of mixtures reported as nominal 0.01, 0.1, 1, 5, and

10 ml/L, as previously described). They found that at the highest

concentrations of 1, 5, and 10-ml/L settlement of planulae was significantly

lower than in the controls.

Epstein et al. (2000) used the earlier experiments of Bak and Rinkevich, and

Rinkevich and Loya, as a basis to examine the effects of both oil and dispersant

exposure to the planulae of Stylophora pistillata and the soft coral Hetertoxenia

fuscescense. For oil effects, they prepared a WSF mixture of Egyptian crude oil

by shaking a 1:200 mix of oil:water overnight and used this as a stock solution

for dilutions. Over a 96-hr exposure period, no S. pistillata mortalities were

observed in any dilutions from 0.1-100 percent of the stock WSF mix.

However, significantly fewer settlements of S. pistillata planulae occurred.

There were no observed abnormalities in settled polyp morphology or in

larvae swimming behavior.
42

Kushmaro et al. (1996) used the planulae of Heteroxenia fuscescense to study

the effect of crude oil (unspecified) on metamorphosis. The crude oil was

both floated on the water surface and used as a coating on the test vessels.

Only nominal, not measured, exposure concentrations of oil were provided.

In both exposure scenarios the nominal concentrations ranged as high as 5000

ppm.

With increasing concentration of oil on the water’s surface, planulae

increasingly lost the ability to undergo metamorphosis to polyps. At 10-ppm

nominal crude oil, for example, only 50 percent metamorphosis occurred

(compared to 97 percent in controls). The remaining planulae survived and

appeared normal but did not metamorphose. Acute mortality of planulae

increased at 500 ppm and above.

Oil coating on the experimental containers’ surface also inhibited

metamorphosis, at concentrations as low as 0.1 ppm. Planulae held in

0.1 ppm oil showed a 50 percent metamorphosis rate; at 100 ppm, only 3.3

percent metamorphosed. An increase in morphological deformities was also

observed.

Kushmaro et al. felt that mortality was not a sensitive indicator of crude oil

toxicity in H. fuscescense, and recommended consideration of sublethal effects

at lower concentration ranges.

As previously described, Te (1991) exposed the planulae of Pocillopora

damicornis to different nominal concentrations of gasoline:oil mixture and to

benzene. Acute toxicity was noted only at the highest exposure

concentration (100 ppm) in the closed system experiment. Clear

correlations between concentration and settlement rate (corallite formation)

were not evident with the gasoline:oil mixture. Te commented that the

actual concentration per container may have varied significantly from one

another—as we have naggingly noted, one of the primary problems with the

use of nominal concentrations.

Results in the benzene exposures were similarly variable and difficult to

interpret. In fact, Te suggested that the settling response in corals may not be

suitable as a bioassay for exposure to petroleum hydrocarbons. He further

recommended that future studies incorporate quantitative measurements of

exposure, as opposed to the nominal or calculated equivalents.

In addition to the fertilization assays detailed previously, Negri and Heyward

(2000) assessed the effects of crude oil and dispersant WAFs to Acropora

millepora recruitment as reflected by inhibition of metamorphosis. In contrast

to the findings of Te above, Negri and Heyward determined that

settlement/metamorphosis to be a useful assay for exposure to oil. The

results indicated that the larval metamorphosis assay was more sensitive to

crude oil WAF than was the fertilization test. Crude oil significantly inhibited
43

larval metamorphosis at 0.0824 ppm total hydrocarbon concentration, and

completely inhibited it at 0.165 ppm. The dispersed oil mixtures (1 and 10

percent dispersant:oil used for stock WAF preparations) significantly inhibited

metamorphosis at 0.225 ppm and 0.0325 ppm, respectively.

Histological Changes 

Peters et al. (1981) performed a three-month laboratory exposure of the

shallow-water Caribbean hermatypic coral species, Manicina areolata, to No.

2 fuel oil. Over the experimental period, none of the corals died. However,

other physiological and histological changes were noted. At two, four, and six

weeks into the study, corals showed increased mucus secretory cell activity.

Both numbers and size of these cells increased until the eighth through

twelfth weeks. At this point, the secretory cells atrophied and in some cases

disappeared altogether. Other histological and cellular changes were

observed as well, including loss of symbiotic zooxanthellae from the

gastrodermis and mesenteries.

The authors suggested that because corals have a high lipid content, oil may

partition into cells or membranes to disrupt vital bioenergetic processes and

the symbiotic relationship between coral host and zooxanthellae.

Calcification and Growth (Extension) Effects 

Researchers such as Birkeland et al. (1976) stated that in the absence of acute

mortality effects in coral from oil, evaluating the rate of growth provides

probably the best quantitative, objective measure that integrates a variety of

physiological effects. To that end, they collected heads of Porites furcata in

Caribbean Panama and performed a series of oil exposure experiments.

Birkeland et al. exposed heads of P. furcata to Bunker C oil for periods of 1

and 2.5 hrs, after which the colonies were placed back in the field for 61 days

(controls were also established in which colonies were held in clean seawater

with no oil added, for the same exposure time periods). As has been

common for many of the earlier coral and oil toxicity studies, the actual

exposure concentration was not measured. In this study, even the nominal

concentration was not specified: only that 100 ml of Bunker C was added to

buckets containing coral colonies and “just enough seawater to cover them.”

The resultant oil film on the surface of the water was noted at 2.4 mm in

thickness.

Twenty-four hours following placement in the field, all colonies were

examined and appeared healthy. After the two-month post-exposure

periods, growth measurements were taken on the calcareous skeletons of

control and treated corals .
44

Interestingly, the authors noted no visible qualitative differences between

control and Bunker C exposed corals (i.e., no apparent damage), but the

difference in growth increments was significant. Further, a significantly

greater proportion of branches among the oiled corals failed to grow at all.

Neff and Anderson (1981) examined several sublethal endpoints with a range

of oils and constituents (No. 2, South Louisiana crude, phenanthrene,

naphthalene) on four species of scleractinian corals (Madracis decatis; Oculina

diffusa; Montastrea annularis; Favia fragum) and one species of hydrocoral

(Millepora sp.). Although only a few of the experiments included a flowthrough exposure design, actual exposure concentrations were measured or

estimated by IR spectrometry or conversion of radioactivity.

Among the investigations on corals, Neff and Anderson studied the effect of

water-soluble fraction of No. 2 fuel oil on calcium deposition in Oculina

diffusa. They found a high degree of variability in the depositional rates, but

noted a trend of decrease in rates with decreasing WSF concentration.

Overall, Neff and Anderson found that exposure to 0.45 and 0.87 ppm total

hydrocarbons resulted in approximately 60 percent reduction in 45Ca

deposited by O. diffusa in 3 hrs.

They also performed experiments with five species of Bermuda reef corals

and WSF of No. 2 fuel oil and South Louisiana crude oil. Results were quite

variable. In some cases, (Millepora sp.), there was a trend (but not significantly

so) toward increased 45Ca deposition rates with increased concentration;

Favia fragum was unaffected; Madracis decatis showed trends both toward both

increased and decreased Ca deposition in different experiments, but

significant results were obtained only in isolated instances. One experiment

was performed with M. decatis and WSF of South Louisiana crude and the rate

of calcium deposition was found to increase significantly with increasing WSF

concentration. In Monastrea annularis, 45Ca deposition increased slightly with

exposure to No. 2 fuel oil, but only one significant result was obtained in the

immediately post-exposure studies and with a 72-hr recovery period.

No. 2 fuel oil WSF significantly depressed calcium deposition in Oculina diffusa

at the 2.6-ppm concentration but not at lower levels. Again, however,

variability was high.

Exposure to phenanthrene resulted in both increased and decreased Ca

uptake in Millepora sp., depending on concentration: lower levels (25 ppb)

resulted in a great increase, while 100 and 500 ppb caused a slight decrease;

variability was high.

Gardiner and Word (1997), and Gardiner et al. (1998) exposed colonies of

Acropora elsyii to WAFs of a condensate and crude oil for 144 hrs, as detailed

above under acute effects (refer to Table 2 to obtain approximate

hydrocarbon concentrations for WAF mixtures of the two products). They
45

obtained what can best be described as a variable set of growth (wet-weight

biomass increase) responses under the different conditions of exposure:

growth relative to controls was suppressed by one-third and two-thirds in the

full-strength solutions of 150°C and 200°C weathered Campbell condensate,

and “variable” among the diluted concentrations of the weathered condensate

WAFs (recall that the full-strength fresh condensate WAF was acutely toxic

to the corals). Growth was enhanced in the 10 percent WAF of the 200°C

weathered Stag crude oil; inhibited in the 100 percent WAF from fresh Stag

and 10 percent WAF of 200°C weathered Stag; and unaffected in the 50 or 100

percent WAFs of the 200°C Stag.

Dodge et al. (1984) attempted to simulate spill-like conditions by exposing

colonies of Diploria strigosa collected in Bermuda to various concentrations (1-

50 ppm, measured in water by fluorescence spectrometry) of Arabian Light

crude oil for 6-24 hr periods in four laboratory and two field experiments.

Following the exposure, the corals were moved to/left in place in the field for

approximately one year. At that time, extension (growth) of skeletons was

measured. This experimental design was intended to assess the long-term

effects of a brief low-level exposure, as would be expected during an oil spill.

Dodge et al. found no effects of the oil exposure to D. strigosa. However, this

should be tempered with the observation that substantial natural variability in

growth parameters existed for the corals, which compromised the ability to

detect small changes.

As a component of post-spill effects monitoring, Guzmán et al. (1991) and

Guzmán et al. (1994) reported the results of coral growth studies

(“sclerochronological analysis”) after the Bahía Las Minas spill in Panama in

four native coral species. Initially, Guzmán et al. (1991) found reductions in

growth for three of the species (P. astreoides, D. strigosa, and M. annularis) and

no effect in one (S. siderea). The lowest annual mean growth rates were

measured for 1986, the year of the spill. Five years later, Guzmán et al.

(1994) examined growth rates in S. siderea and P. astreoides. Growth rates for

both were lower during the three years after the spill than before. At heavily

oiled reefs, growth after the spill declined significantly for S. siderea but not for

P. astreoides.

A more general study of coral growth by Lough and Barnes (1997) provides

excellent background on the use of skeletal extension and density banding as a

means to document environmental changes over time. They discuss both the

advantages of using massive corals in this way as well as the drawbacks and

limitations. Their review and research make it clear that oil spills are but one

kind of environmental change that can affect coral growth. In studying massive

Porites colonies (the skeletal cores could not be identified to species) on the

Great Barrier Reef, Lough and Barnes found a particular sensitivity to sea

surface temperature, with higher temperatures resulting in higher calcification
46

and lower temperatures in lower calcification. However, they cite other

research demonstrating growth impacts from bleaching, sewage, offshore

drilling, dredging, eutrophication, and oil spills. They noted that because the

links between environmental factors and density banding have been mostly

through correlation rather than mechanistic studies of how environmental

conditions affect growth, those links have been uncertain and “fuzzy.”

Among oil spill researchers, Birkeland et al. cautioned that differences in

spatial location of colonies, and time of year, each affected growth rate to a

greater extent than did the exposure to oil. Neff and Anderson, despite

concluding that 45Ca deposition was a sensitive indicator of contaminantinduced stress in corals, noted that the high variability they experienced during

the course of their experiments was a problem. However, they suggested

that increasing the sample size and standardizing other experimental

parameters would partially compensate for this and permit the use of the

parameter.

Given the fact that several of the researchers using coral growth as an

indicator of effect commented on interpretive complications and limitations

due to natural variability and the influence of other environmental stressors

and influences independent of oil, this may not be the best standalone

endpoint for evaluation of spill impacts on a coral community. However,

because growth integrates several parameters related to the overall health of

a colony, it would seem reasonable to include it as part of a suite of endpoints

in a multivariate assessment.

Surface Cover 

Changes in coral cover over time represent another way to assess longerterm conditions in a reef. Similar to the use of coral growth results to infer

oil spill impacts, relying exclusively on coral cover may not provide spillspecific insights. However, it should reflect an integrated response to

environmental conditions that can include an oil spill.

Guzmán et al. (1991) compared cover of common coral species (noted

elsewhere) at six reefs before (1985) and after (3 months post) the oil spill at

Bahía Las Minas. At one heavily oiled reef, total coral cover decreased by

76 percent in the 0.5-3 m depth range and by 56 percent in the >3-6 m range.

The decrease in cover was less at moderately oiled reefs and either increased

or did not change at the unoiled reference reefs. The branching species

Acropora palmata nearly disappeared at the heavily oiled site, but increased by

38 percent at the unoiled reefs.

In this same survey, Guzmán et al. also documented changes in average size of

colonies and diversity based on cover. They found that colony size and

diversity decreased significantly with increased oiling.
47

The TROPICS experiment (Ballou et al. 1987; Dodge et al. 1995) in Panama

used changes in coral cover as one measure in assessing short- and long-term

effects of oil and dispersant use in the three tropical habitats of mangroves,

seagrass, and coral reefs. A slight, but statistically significant, decrease in coral

colony cover was found over the period immediately following the oil

exposure through 20 months, but when the site was revisited ten years later

the difference in this measure relative to unoiled control had disappeared.

Photosynthesis 

The symbiotic relationship between reef-building corals and their associated

dinoflagellate algae (zooxanthellae) is well known, and the expulsion of the

symbionts under stressful environmental conditions (bleaching) has been the

source of much recent concern. As summarized by Benson and Muscatine

(1974), the presence of zooxanthellae is not insignificant, either physically or

functionally: in the coral Pocillopora damicornis, the algae constitute 45-60

percent of protein biomass of the colony; and, they provide the animal with

photosynthetic products such as glycerol, alanine, and glucose. In turn, the

coral supplies the algae with ammonia and protein.

Given the importance of the symbiotic relationship to the health of corals and

the reef community, the effect of oil on photosynthesis represents a key

series of endpoints for consideration. Cook and Knap (1983) studied the

effect of Arabian Light crude oil and the dispersant Corexit 9527 both

individually and in concert on the brain coral, Diploria strigosa. In this case,

fluorescence spectrometry measured exposure concentrations in the water;

average concentrations were 18-20 ppm and the dosing curve was similar to

that illustrated in Figure 2. These, according to the authors, represented

realistic upper limits to concentrations that might be encountered on a reef

during a real spill in which dispersants were applied. Photosynthesis (carbon

fixation) was studied using radioactive carbon.

Exposure to Arabian crude oil alone did not affect carbon fixation, expressed

as total carbon fixed, in the distribution of labeled carbon in different chemical

fractions of coral tissue, or in the distribution of photosynthetic carbon into

lipid classes. Although some short-term (1-3 hrs after dosing) significant

impacts to photosynthesis were noted with oil + dispersant, the reader is

referred to the Cook and Knap article for detailed discussion.

Cook and Knap concluded that their results suggest that, without the

application of dispersants, oil pollutants in realistic environmental

concentrations had little effect on coral photosynthesis.

Cook and Knap compared their results to those of Neff and Anderson (1981)

and commented that experimental approaches differed in important ways,

such as longer dosing periods in static systems in the latter study, different

oils and concentrations, and different methods of tissue digestion. Despite
48

the methodological differences, Cook and Knap concluded that both studies

found little substantive impact to coral photosynthesis from oil exposures at

“realistic environmental concentrations.” However, Neff and Anderson did

determine that exposure of fire coral (Millepora sp.) to the water-soluble

fraction of No. 2 fuel oil for 72 hrs resulted in a highly significant reduction in

the rate of photosynthetic carbon fixation by zooxanthellae. They found a

linear relationship increasing WSF concentrations and decreasing 14C uptake

rate, with exposure to 2.6 ppm total hydrocarbons resulting in an

approximately 50-percent decline. If corals were permitted to recover for 72

hrs, the effect appeared to be transient and no differences could be detected

between control and exposed specimens.

Interestingly, qualitatively different results were found for the species

Madracis decatis. That is, after 72-hrs exposure to WSF of No. 2 fuel oil, no

difference was found in the rates of carbon fixation. However, after another

72 hrs of post-exposure recovery, there was a significant and inverse

relationship between previous exposure concentration and 14C fixation rate:

previous exposure to 2.6 ppm total hydrocarbon produced a 60-percent

decrease in carbon fixation rate.

In 24 hr exposure tests with No. 2 fuel oil and South Louisiana crude oil, Neff

and Anderson found no effect in the zooxanthellae of Favia fragum and

Montastrea annularis. Inhibition of carbon fixation was found when Millepora

sp. was exposed for 24 hrs. to phenanthrene, with a maximum decrease of

54 percent correlated with an exposure of 500 ppb.

Despite the findings of some impact to photosynthetic carbon fixation by

coral zooxanthellae from exposure to oil, Neff and Anderson concluded that

relative to oil effects on free-living marine algae, the coral zooxanthellae were

“not greatly affected” by sublethal exposure.

Gardiner and Word (1997) determined that exposure of Acropora elsyii to two

of the three full-strength WAFs of fresh and weathered Campbell condensate

and all three WAFs of Stag crude oil resulted in substantial reductions in

levels of chlorophyll a within coral tissues. However, only one of the

dilutions (50-percent concentration of fresh Campbell condensate) caused a

reduction.

Rinkevich and Loya (1983) also studied the effect of crude oil (Iranian) on

photosynthesis of the branching coral, Stylophora pistillata. For this series of

experiments they prepared a stock water-soluble fraction mix of the crude oil

by mixing 300 ml of the Iranian crude with 700 ml of filtered seawater. This

was stirred for 24 hrs, allowed to stand for 30 minutes, after which the water

was drained and designated as 100 percent water-soluble fraction. Dilutions

of 2.5-20.0 ml WSF/L were prepared and used. Corals were incubated with

Na2

14CO3 in 3 m of water in the Red Sea.
49

No mortality was observed to corals or zooxanthellae. However,

photosynthesis was affected: a decrease in higher (12.0 ml/L) WSF

concentrations, and an increase at lower concentrations. Rinkevich and Loya

interpreted the latter phenomenon (increase in photosynthesis at low-level

exposures to WSF of crude oil) as a stress reaction called hormesis. The

authors also suggested that these results reflect the inadequacy of traditional

dose-response models due to the “toggling” of stimulation and inhibition with

dose.

Mucus and Lipids

We might think of mucus as a physiological by-product rather than an

important constituent in reef ecosystem energetics, but several researchers

have studied the role of coral mucus and the impacts oil exposure might have

on production and energy transfer in the reef. There is, in fact, a surprising

amount of information on coral mucus and oil effects in the literature.

Benson and Muscatine (1974) researched the basic chemistry of coral mucus

and also studied feeding behavior of reef fishes on the material. They found

that coral mucus was rich in wax esters and triglycerides. In addition to

observing fish feeding directly and extensively on mucus, they also found that

artificially dispensing coral mucus resulted in an aggregation and feeding by

fish. That is, reef fish like coral mucus. Benson and Muscatine suggested that

ingestion of coral mucus by reef fishes was a likely route for the energy-rich

products of coral metabolism to be transferred into the larger reef system.

Mitchell and Chet (1975) exposed healthy corals heads of the genus Platigyra,

collected in the Red Sea, to crude oil and other chemicals. Unfortunately,

little specific information is provided about the specifics of crude oil type and

the manner in which the coral was exposed to oil. With this qualification in

mind, they observed that addition of crude oil caused a dramatic increase in

the production of mucus: 100 ppm crude oil increased production from 25 to

500 μg/10 ml over the 24 hr. test period, while 1000 ppm caused an increase

in mucus production from 30 μg to 600 μg in the first day. In the latter

exposure, mucus production subsequently declined to 100 μg after 4 days and

remained at that level until the corals died on day 6. Exposure to other

chemicals suggested that increase in mucus production was a generalized

reaction to pollution stress.

Harrison et al. (1990) exposed a staghorn coral, Acropora formosa, collected

from the Great Barrier Reef, to 5 and 10 ppm water-accommodated fraction

of marine fuel oil (among other stress treatments, including

chemicallydispersed oil and dispersants alone). Exposure concentrations

were measured gravimetrically (i.e., water samples were filtered, extracted

three times in dichloromethane, evaporated, and residues were weighed). In

both oil treatments, response of the coral was similar: “massive” amounts of

mucus were immediately discharged during the first hour of treatment.
50

Branches were able to withstand a 6-hr exposure, but some died after a 12-hr

exposure. After 48 hrs, the authors noted a marked increase in the

concentration of pigmented bacteria on the mucus, which they attributed to

increased amounts of mucus and possibly to bacterial utilization of oil

components.

Cook and Knap (1983) summarized the role of symbiont photosynthesis in

corals and in reef ecology by noting that the primary production by

zooxanthellae probably provides most of a coral’s energy requirements.

They linked primary production, mucus, and energy dynamics in the larger

reef community by the same route described by Benson and Muscatine above.

Burns and Knap (1989) found indications that corals heavily stressed by oil had

altered protein to lipid ratios and they discussed the adverse implications of

impacts to lipid metabolism. As an example, they noted that a large portion

of the energy fixed in algae/coral photosynthesis was channeled into mucus

production. Mucus, with its high-energy lipid-rich content, was acknowledged

to be a key component in reef food web bioenergetics, and Burns and Knap

suggested that impairment of lipid metabolism in corals induced by oil

exposure could easily cascade into the larger reef ecosystem.

Neff and Anderson (1981) made a qualitative observation of increased mucus

production in Montastrea annularis with exposure to South Louisiana crude

oil. Although they did not quantify the amount of production, they did use UV

spectrophotometry to target naphthalenes in mucus. Naphthalenes were

detected. Similarly, after exposure to 14C-naphthalene, Neff and Anderson

detected 14C in mucus produced by M. annularis. They suggested that the

results indicate that:

• Coral mucus can bind or adsorb aromatic hydrocarbons;

• Surface mucus may protect coral tissues from aqueous hydrocarbons;

• Mucus production may be a mechanism of hydrocarbon clearance from

contaminated corals.

To explore the idea that coral mucus may act to transfer both energy as well

as hydrocarbon exposure to the larger reef ecosystem, Neff and Anderson

also studied the reef-dwelling butterfly fish (Chaetodon sp.). The fish was

observed to actively ingest coral mucus. Corals exposed to WSF of South

Louisiana crude for 24 hrs were placed in aquaria with butterfly fish, which fed

on the mucus produced by the corals for several hours. Although low

concentrations were found in several organs of the fish and in coral tissues,

relatively high levels were found in gall bladder (5.77 ppm wet weight), head

(4.51 ppm), heart (2.47 ppm), and brain (1.62 ppm) tissues.

These studies indicate that the relationship between coral mucus and oil

exposure is a complex one. Researchers have shown that mucus production

varies with oil exposure and that it may be a vehicle for removal from coral
51

colonies. However, the high lipid content of mucus and its role as a food

source to other organisms would suggest that in the event of oil exposure,

mucus would also be a ready pathway to transfer not only energy, but also

contamination.

OTHER EFFECTS OF OIL: BIOACCUMULATION

Oil quickly and readily bioaccumulates in coral tissues and is slow to

depurate. This may be linked to the high lipid content of the tissues.

Uptake into the symbiotic zooxanthellae also occurs. Researchers

have found that petroleum hydrocarbons are deposited into the

calcareous (aragonite) exoskeleton of corals, which introduces the

possibility of using coral skeletons as historical records of

hydrocarbon contamination in an area.

Bioaccumulation—defined as the concentration of a chemical in an organism

through uptake from water or ingested food—has been studied in the context

of oil and corals by many researchers.

We alluded to the lipid constituent in coral mucus above. Harriott (1993)

reviewed studies of the role of lipids in coral histology and physiology and

noted that lipid deposits were likely to be important energy reserves for the

animals. The known affinity of petroleum hydrocarbons for lipid-rich tissues

would imply the likelihood of bioaccumulation occurring when corals are

exposed to oil.

Harriott had hoped to utilize the lipid content of corals from the Great

Barrier Reef in an index for general condition (she had noted that lipid decline

had been previously used to monitor changing condition of marine organisms,

including corals). However, she commented that the method required a

considerable refinement to achieve consistent results; and even when this

took place, there was considerable variation among samples from the same

colony. In addition, the efficacy of lipid extraction varied between species

(Pocillopora damicornis and Acropora formosa). Harriott concluded that the

approach was problematic, not necessarily from a conceptual perspective, but

rather from an applied standpoint.

In the chronic laboratory exposure of M. areolata by Peters et al. (1981)

discussed above, the No. 2 oil was mixed with seawater with targeted wateraccommodated fraction (WAF) of hydrocarbons of 0.1 ppm and 0.5 ppm.

Measured concentrations for the two targets were 0.07 ± 0.04 ppm and 0.15

± 0.10 ppm, respectively.

Chemical analysis by GLC/FID showed probable increases in coral tissue

hydrocarbons from exposure to the WAFs after two weeks in the higher

exposure concentration and six weeks in the lower. After one to two weeks
52

of elimination*

 time in clean flowing seawater, all corals retained oilassociated hydrocarbons in their tissues. The lighter fractions, however,

appeared to have volatilized or solubilized.

In addition to studying the lethal and sublethal effects of Iranian crude oil to

the octocoral Heteroxenia fuscescens, Cohen et al. (1977) also evaluated uptake

of petroleum hydrocarbons by the test colonies. While they demonstrated

through examination of gas chromatograms that the corals were

incorporating petroleum-derived hydrocarbons into tissues, the actual

amount of uptake was not specified; it was noted as being much lower than

“normal hydrocarbon background.”

Knap et al. (1982) used a radioactive form of the polynuclear aromatic

hydrocarbon (PAH) phenanthrene ([9—14C] phenanthrene) to document

uptake and elimination in the coral Diploria strigosa collected from the

northern fringing reefs of Bermuda. Knap et al. used an exposure

concentration equivalent to 33 ppb and found that, after a one-day exposure,

about 17 percent of the radioactivity in the water were incorporated into the

coral. The corals were then allowed to eliminate the radioactive

phenanthrene in clean seawater. A sharp decrease in radioactivity was

observed after the first two days of elimination, which was followed by a

much slower rate through the rest of the 14-day experiment. At day 10 of

elimination about 25 percent of the initially accumulated radioactivity was still

present.

Other researchers have observed this kind of uptake and elimination pattern

in other species of coral. Kennedy et al. (1992) tracked the fate of the PAH

[3H]benzo[a]pyrene (BaP) in two scleractinian coral species, Favia fragum and

Montastrea annularis, collected from Biscayne National Park, Florida. They

confirmed that corals accumulated BaP in their soft tissues, and were also able

to show that the symbiotic zooxanthellae sequestered it as well.

They found that both F. fragrum and M. annularis readily incorporated the

radioactive BaP from water, with a strong linear relationship shown between

uptake rate and concentration of BaP. Normalized to skeletal surface area, M.

annularis showed an uptake rate that was roughly twice that for F. fragrum.

Similar to the findings of Knap et al. (1982), elimination of BaP from both

species was slow, with a more rapid rate in the first 50 hrs than the last 94

hrs. At the end of the 144-hr experiment, F. fragrum had eliminated over half

of its accumulated BaP, but M. annularis still retained about 60 percent.

 

*

 We follow the suggested practice of Meador et al. (1995), in which the word depuration is

reserved for passive processes of contaminant reduction in an organism, such as diffusion;

and use elimination for the combined processes of metabolism, excretion, and diffusive loss

of contaminants.
53

BaP-derived radioactivity was found in both the coral animals and the

zooxanthellae fractions. The proportion in coral tissue vs. zooxanthellae

fluctuated considerably with time, and differences were also noted between

species.

Kennedy et al. found a relatively low proportion of the radioactivity in both

coral tissue and zooxanthellae in an aqueous-soluble phase, which they say

suggested only a limited ability to biotransform and detoxify BaP. Although

this might reduce the toxic effects attributable to reactive BaP metabolites, it

also would suggest a prolonged exposure to the parent compound.

In field studies stemming from the 1986 Bahía Las Minas oil spill in Panama,

Burns and Knap (1989) confirmed laboratory observations of coral

bioaccumulation in the two species Siderastrea siderea (a massive species) and

Agaricia tenuifolia (thin, plate-like colonies).

Based on the residue patterns from the gas chromatograph, the corals

appeared to take up hydrocarbons from the water column, as opposed to

sediments. Coral mortality data, as shown by decrease in coral cover,

correlated with hydrocarbon concentrations from surviving coral tissues.

Neff and Anderson reported less conclusive evidence of hydrocarbon

(naphthalene) uptake in three species of corals from Florida (Montastrea

annularis, Acropora cervicornis, and Acropora palmata). They exposed colonies

to a surface slick of South Louisiana crude oil for up to three days. There was

no direct contact, only exposure to dispersed and soluble fractions of the

crude at naphthalene concentrations that ranged between 0.006 and 0.29 ppm

in a flow-through exposure setup. Neff and Anderson did not find a significant

accumulation of naphthalene in the exposed corals, and no aromatic

hydrocarbons were found by gas chromatograph at or exceeding 0.1 ppm.

Oil-exposed corals did contain higher concentrations of total hydrocarbons,

with the difference attributed by Neff and Anderson to increased

accumulation and production of paraffin-type compounds in oil-exposed

colonies. They suggested that oil-induced stimulation of wax-rich mucus may

have been a contributing factor in this increase.

In another experiment by Neff and Anderson, Oculina diffusa from Texas was

exposed to a 10-percent solution of South Louisiana crude oil spiked with

14C-naphthalene estimated to provide an exposure concentration of

naphthalene of about 42 ppb. Although initial concentrations of naphthalene in

the exposure medium declined rapidly (50 percent loss of the spiked material

in 3 hrs, 74 percent loss after 7 hrs), uptake of the naphthalene into coral

tissues was rapid (Figure 3). The maximum radioactivity was estimated to

equal about 0.27 ppm naphthalene/protein N. An elimination curve indicated

that accumulated naphthalene would be cleared in 14 days; the half-time (t1/2)

of naphthalene elimination was about 24 hrs.
54

200

160

120

80

40

0

1 2 46 1 2 4 68 10 20 40 60 80100 200

14C-Naphthalene (CPM/mg protein)

Hours

UPTAKE DEPURATION

Figure 3. Accumulation (during 7-hr exposure to spiked WSF of South

Louisiana crude oil) and elimination (following return to clean

seawater) of 14C-naphthalene by Oculina diffusa. From Neff and

Anderson (1981).

Neff and Anderson (1981) also studied the differences in 14C-naphthalene

uptake in Madracis decatis under light or dark conditions. The coral

accumulated significantly more naphthalene in the light than in dark, although

they noted a high level of variability especially under light conditions.

Although we typically think of bioaccumulation as occurring in soft tissues, it

can also include the bony or skeletal portions of an organism as well.

Readman et al. (1996) studied corals in the northwestern Arabian Gulf

(Kuwait and Saudi Arabia) after the 1991 Gulf War and found that the coral

Porites lutea incorporated oil into the calcareous exoskeleton. The coral

materials were sectioned and dated using microscopic and x-ray inspection.

Chemical analysis for aliphatic hydrocarbons was accomplished by GC-FID,

while the aromatic hydrocarbons were analyzed by GC/MS. Combining the

dating of coral layers with the detailed chemistry within layers, Readman et al.

were able to confirm that the colonies did incorporate hydrocarbons that

fingerprinted back to the oil types known to have spilled during the Gulf War.

Although they state that the occlusion process, as they termed the

incorporation of hydrocarbons into the aragonite exoskeleton, is not fully

understood, the elevated concentrations found within the skeleton likely

reflect enhanced exposure at the time of deposition. However, they noted

that selective degradation processes also seemed to occur, and that further

work was necessary to confirm whether occlusion is proportional to

exposure. This would determine the usefulness of corals as historical

recorders of organic markers.
55

Guzmán and Jarvis (1996) conducted a similar study to that of Readman et al.

above, but used the presence of the element vanadium in coral (Siderastrea

siderea) skeletons as a proxy for oil exposure (vanadium is found as a trace

compound in crude oils). Guzmán and Jarvis used the skeletal incorporation

of vanadium as a potential indicator of chronic oil pollution attributable to the

operation of an oil refinery in Panama, and found a good correlation between

increase in concentration and the beginning of refining activities. They suggest

that vanadium could also be used to document the longer-term history of

regional oil contamination.

In addition to actually incorporating compounds to which they are exposed

into their skeletons, corals record physical evidence of injury and recovery

into their growth rings. Ruesink (1997) used these “scars” and

“sclerochronology” (defined as the study of scleractinian coral growth rings),

in the skeletons of two scleractinian species, Siderastrea siderea and Porites

astreoides, to evaluate susceptibility to injury and ability to recover from it.

The colonies had been collected to assess the effects of the Bahía Las Minas

spill, but the results of Ruesink’s study were not directly applicable to impact

assessment from that particular incident. In fact, although Ruesink concluded,

based on her sclerochronology study, that P. astreoides sustained less injury to

internal regions of the colony and recovered more quickly than S. siderea, she

was able to discern no obvious trends in injury rates over the preceding

several decades, even at the site of several oil spills. Ruesink noted that the

significant drawbacks to sclerochronology as a means to document

disturbance in the coral reef system derive from what is not preserved in the

skeletons: i.e., small, rapidly recovering injuries, and total colony death. This,

unfortunately, may preclude two of the major effects observed as oil spill

effects in corals and thus probably limits the utility of the approach in a

disturbance assessment context.

INDIRECT IMPACTS

The indirect impacts of exposure to oil or to oil spill activities can take many

different forms, only a few of which we will detail here. It should be clear by

now that oil directly affects corals in a number of ways, but it can also initiate

a sequence of events that ultimately can result in an endpoint of damage to the

coral reef. We can find indications of this from laboratory work as well as

field observations.

As detailed previously, Mitchell and Chet (1975) documented that exposure

to crude oil caused corals to increase their production of mucus. They also

studied the role of bacteria in determining the severity of impact from the

production of the excess mucus. Interestingly, they found that coral mortality

occurred only in the presence of bacteria and, when microbial growth was

inhibited or prevented through the addition of antibiotics, the corals survived
56

exposure to the chemical contaminants. Mitchell and Chet suggested three

different microbial mechanisms for death of the coral:

1. Predatory bacteria were initially attracted to the excreted mucus, which

then attacked the coral tissue;

2. Bacteria of the genus Desulfovibrio, attracted to reduced redox conditions

produced by the growth of other bacteria, produce hydrogen sulfide,

which possibly killed the corals;

3. Infected corals were visibly covered with a filamentous bacterium called

Beggiatoa, a heterotrophic genus that may have fed on the coral tissue

itself.

Mitchell and Chet concluded that pollutant concentrations insufficient to kill

corals directly can cause death indirectly by stimulating adverse microbial

processes.

Harrison et al. (1990) observed a similar “bloom” of bacteria on the increased

mucus production from Acropora formosa corals exposed to WAF of marine

fuel oil. Although they cautioned that the extent to which the bacteria caused

the destruction of coral tissue was not known, they felt it likely that the

increased microbial activity contributed to the collapse of the tissue.

However, they also postulated that this bacterial action may have been an

artifact of the experimental setup. That is, in normal reef environments the

mucus and bacteria would be carried off the coral or ingested by reef

dwellers; in a tank with static or insufficient flow-through conditions, the

bacterial population could rapidly rise above normal levels and result in

additional coral stress.

Kinsey (1973) studied another phenomenon associated with oil spills that

could conceivably affect corals in an indirect way, the effect that crude oil

slicks might have on gaseous exchange over a reef. The author asserted

that—at least in some reefs, such as the Great Barrier—corals have an oxygen

requirement so critical and sensitive to change that extreme tides in sheltered

reefs can sometimes result in completely anoxic conditions with resultant

mortalities to much of the community.

Kinsey used a Moonie crude oil to create slicks with approximate thicknesses

of 0.1 and 0.7 mm. He found that while the oil caused a noticeable calming of

the water surface, there was no interference with normal gas exchange

(specifically, oxygen and carbon dioxide) between the water and atmosphere,

and hence, no adverse impact.

Recent work has elevated the level of concern related to photoreactivity of

petroleum hydrocarbons to greater prominence. Although at this writing, no

research specific to corals has taken place, results to date suggest an area for

future work and the potential for significant adverse impact during oil spills.

Pelletier et al. (2000), for example, found that maternal transfer of the PAH
57

fluoranthene (a common component of petroleum products) from adult

bivalves to pelagic larvae occurred and then rendered the larvae susceptible to

photoxicity effects when they were in the water column. The demonstrated

ability of corals to accumulate PAHs and, perhaps more importantly, the

strength and duration of sunlight exposure in the clear, shallow waters

typifying coral reef environments should flag possible photoreactive toxicity

effects as a concern during spills.

Finally, there is an indirect consideration that has received little attention in

the coral and oil literature but is well known to spill responders. A sensitive

resource like a coral reef can be damaged by the response and cleanup itself.

Ray (1981) noted this in closing his review of oil spill impacts, and singled out

resuspension of sediments by propellers and mechanical damage from boats,

anchors, and personnel as potential sources of damage that could take years

to recover. In many cases, cleanup-related impacts can be minimized or

reduced with awareness and planning, but rarely are they completely

eliminated.

VARIABILITY IN IMPACT DUE TO REPRODUCTIVE

STRATEGY

The vulnerability of gametes and early life stages of coral to oil suggests that

there is a critical link between timing of a spill and the nature of coral

reproduction to determine impact. In many, if not most, organisms, the

earlier developmental stages often do not have fully functional detoxification

mechanisms and are less capable of dealing with toxic exposure than are

more mature forms of the same organism. Many of the studies previously

reviewed documented effects of oil on coral fecundity or planulae. As pointed

out by Guzmán and Holst (1993), the gametes of most spawning marine

species tend to rise to the surface of the water after spawning. Negri and

Heyward (2000) noted that coral oocytes are rich in hydrocarbons and highly

buoyant. In mass spawnings such as those typical of the Great Barrier Reef,

these oocytes can form their own slicks in calm weather and there is a high

probability of coral gametes and petroleum products coinciding in the water

column. Moreover, the larval stages of coral spend one to several weeks as

plankton before developing to the point of settling competently. Therefore,

the timing of an oil spill relative to the reproductive cycles of coral species of

concern could be expected to play a key role in determining the impact to the

population. Presumably due to their inherent tendency to associate with the

uppermost layers of the water column, free-floating larvae stand a greater

chance of contacting elevated concentrations of oil than would larvae that are

not dispersed from the colonies. Empirical information (Pain 1994) from

Bahía Las Minas reflected this, as those coral species with dispersed

planktonic larvae were found to be much less robust than brooding species.
58

Peters et al. (1997) concurred with this idea. They noted that spills occurring

near or at peak reproductive season (e.g., late August in the Caribbean and

Gulf of Mexico, April in the Great Barrier Reef region) could effectively

eliminate an entire year of reproductive effort while continuing to reduce

fecundity through partial mortality and impairment of gonadal development.

In an excellent overview of coral reproduction, Richmond (1987) related how

corals can be hermaphroditic (simultaneous or sequential, and in the latter,

protandrous or protogynous), gonochoric (dioecious), or sterile. Species

may release brooded planulae, spawn gametes, or reproduce solely by asexual

means. It is, however, difficult to generalize about mode of reproduction,

even within the same species: Richmond noted that Acroporis humilis was

reported to brood planulae at Eniwetok, but was found to spawn gametes on

the Great Barrier Reef and in the Red Sea.

In light of these considerations, information on reproduction and recruitment

in various coral species would be a useful reference for spill responders and

resource managers in anticipating potential impacts of a spill incident.

Reviews of this kind of information are uncommon. Fortunately, at least two

exist: Richmond (1987) summarized reproductive data for Caribbean, Pacific,

and Red Sea species, providing information for 92 of what was at that time

estimated to be 400 known scleractinian reef coral species; Richmond and

Hunter (1990) updated and augmented the data to include reproductive

information for 210 of (what was then estimated to be) about 600 identified

corals.

Although data for only about a third of the identified scleractinian coral

species are available, use Appendix C as a quick reference for a broad

geographic region to ascertain whether pelagic coral reproductive activities

are peaking at a given time. See the appendix for more detailed information

on how to use and interpret the information.

VARIABILITY IN IMPACT WITH TIME OF YEAR AND REGION

The time of year in which a spill event occurs overlays on reproductive

strategy to give one predictor of impact. Time of year, independent of

reproductive considerations, is an important determinant of effect for other

reasons, and these are variably intertwined with seasonal weather, geographic

location, and other considerations.

Wyers et al. (1986) found an apparent seasonal difference in the nature of

sublethal oil toxicity in Diploria strigosa. They exposed the coral to a

measured, physically dispersed Arabian oil concentration of 18-23 ppm for a

24-hr period during both summer and during winter months. They found a

qualitatively different kind of impact in the two seasons: in winter, tissue

rupture following exposure was detected in 83 percent of colonies; in

contrast, summertime results included only 22 percent with detectable tissue
59

rupture. Wyers et al. termed these differences in effect “minimal” when

considered over the entire 4-week experimental periods, but also suggested

lower winter water temperature might have contributed to the effects

differences.

Johannes et al. (1972) described a combination of seasonal and regional

factors that may subject a coral reef to greater risk from oil spills . They

mentioned coral reef differences among geographic regions that bear factoring

into response strategies in the event of a spill. For example, they note that

Indo-Pacific reefs include corals that protrude above the water surface on low

tides more commonly than Atlantic reefs. This consideration would certainly

influence the impact that an oil spill of a given size might have on a reef, as a

tidally exposed coral could be expected to suffer more severe impacts from

direct contact with the oil than a coral exposed only to the water-column

fractions of that oil.

During the early days of the Gulf War oil spill in 1991, concerns were raised

about potential effects to the marine environment of the region. In a

background document that detailed threatened resources, the World

Conservation Monitoring Centre (1991) noted that the Gulf is an inherently

stressful environment for corals because it is the northerly range limit for

tropical corals and experiences a wide fluctuation in temperature and salinity.

LeGore et al. (1989) similarly described a seasonal bleaching event in many of

the corals of the Arabian Gulf due to lower ambient water temperatures in

the winter months and suggested an additional susceptibility to oil exposure

because of it.

Jaap et al. (1989) studied the Bird Key Reef coral community in the Dry

Tortugas off Florida and found a similar limitation in reef robustness because

of the low temperatures occasionally encountered during the winter in those

waters. Besides sometimes causing outright mortality due to cold water, the

temperature stresses also were thought to alter reproductive patterns by

inhibiting sexual reproduction. Thus, response-related assumptions about

corals in such an area may not be valid if they are based on general life history

characteristics for a given taxon.

Other scientists and managers have recognized that distinct differences in

tropical marine coastal ecosystems among regions are important. UNESCO

sponsored an entire workshop on the subject in 1986 (Birkeland 1987). In

the proceedings from this workshop, Sammarco (1987) compared ecological

processes on coral reefs of the Caribbean and the Great Barrier Reef and, in

particular, compared coral recruitment patterns in the two areas. He then

discussed these differences in the context of reef recovery from a major

perturbation.

Sammarco focused on corals of a single genus, Acropora, which occurs in both

the Caribbean and in the Great Barrier Reef. Acropora is an important and
60

sometimes dominant genus in both environments. However, distinct

differences exist—especially with respect to recruitment patterns. In the

Caribbean, individuals representing Acropora are rare in the newly settled

community of juvenile corals derived from planulae. On the Great Barrier

Reef, in contrast, newly settled spat from Acropora can account for 50-80

percent of juvenile corals. Sammarco suggested that, in the latter case, most

species of Acropora rely on reproduction via planular settlement, whereas in

the Caribbean, Acropora is more heavily dependent on asexual reproduction

via branch breakage and recementation.

According to Sammarco, the implication, when contemplating recovery of

that genus from a major environmental disturbance, is that the process could

be expected to take longer in the Caribbean than on the Great Barrier Reef.

This suggests that the ability to extrapolate coral biology and disturbance

responses across regions is limited and should be done cautiously. It seems

this is a consistent message across many aspects of coral biology and impact

assessment, as it becomes clear that few hard and fast generalities exist.

VARIABILITY IN IMPACT WITH SPECIES

That inter-species differences exist among corals in toxicity of oil or severity

of spill impacts should not be particularly surprising, since these kinds of

variations in effect have been shown to occur for countless permutations of

organism and contaminant (see, for example, Mayer and Ellersieck 1986).

Some of the studies cited for this report have alluded to potential species

differences in the way oil affects corals. Both Johannes et al. (1972) and

Guzmán et al (1991, 1994) suggested that branching coral species were more

susceptible to oil than non-branching species. Johannes et al. linked the

sensitivity of the branching species—and the increased tolerance of the other

massive species—to the protective qualities of mucus. There may also be

other more subtle factors that contribute to apparent species differences.

Table 3 showed that Bak and Elgershuizen (1976) used impairment in the

ability of corals to clear sediment as an endpoint for sublethal oil toxicity.

Research Planning, Inc. (1986), in a review of the impacts from a ferry

grounding near Isla de Mona, Puerto Rico, suggested that increased

sedimentation from the grounding could affect coral health. They referred to

studies indicating that some species of corals are more sensitive to the effects

of sedimentation and turbidity than others, and identified differences in local

species’ tolerances as follows:

High Sensitivity

Acropora palmata

Acropora annularis

Porites astreoides
61

Intermediate Sensitivity

Diplora labyrithiformes

Diplora strigosa

Montastrea annularis

Madracis mirabilis

Agaricia agaricites

Porites porites

Low Sensitivity

Mussa

Eusmilia

Montastrea cavernosa

Gorgonians

These rankings are independent of any species differences in tolerance to oil,

so it is possible that a vessel grounding could result in negligible detrimental

effects from oil, but cause more severe consequences from the production

and distribution of particulate material in the water column and on the

bottom. It also raises the possibility of synergistic amplification of adverse

impact if oil toxicity combines with indirect effects of the grounding (other

synergistic interactions are discussed in the follow section).

Table 4, previously discussed under Chronic Effects, shows the results of

Lewis (1971). Despite the limitations of the method for calculating oil

exposure, there appeared to be distinct inherent differences in the sublethal

responses of four species of corals, possibly related to the morphology of the

species. Research Planning, Inc. (1986) also made the link between observed

species differences in sensitivity to sediments and physical form by suggesting

that coral species that are cylindrical or upright are less susceptible since flat,

palmate growth forms are more likely to accumulate sediments. In Lewis’

study, however, there were differences in tolerances to oil even between

species of similar form.

Neff and Anderson (1981) had subjected five species of corals to similar oil

exposures and found substantial differences in the resulting toxicities among

the species. They found that Madracis decatis and Montastrea annularis were

severely stressed by exposure to No. 2 fuel oil WSF, as reflected by polyp

retraction, expulsion of zooxanthellae, and marked increase in calcium

deposition. In contrast, Oculina diffusa and Millepora sp. showed no impact in

polyp and zooxanthellae endpoints and a slight decrease in calcium deposition.

The authors did not speculate as to the reasons for these apparent species

differences.
62

SYNERGISTIC IMPACTS

Those who have studied oil spill impacts or other disturbances in natural

systems understand that it is often difficult, if not impossible, to separate the

effects of one perturbation event from others. That is, an area in which we

may wish to study the effects of and recovery from a spill incident may also

have been subjected to one or more natural or human-induced impacts so

that we cannot quantify the relative contribution of each to the resultant

environmental conditions observed.

Dubinsky and Stambler (1996) summarized the range of anthropogenic

stresses to which reef systems are subjected. Their review provides an

appropriately broad framework for considering the impact of oil on corals,

which is but one of many human disturbances to these systems. Moreover,

anthropogenic impacts are a subset of the environmental changes (including

shifts in oceanic conditions and climatic patterns) which ultimately determine

coral reef ecosystem health.

Shinn (1989) was more direct in asserting that anthropogenic influences, while

possibly of local significance, were much less significant than large-scale

influences like sea level change, hurricanes, global increases in carbon dioxide

levels, and changes in water temperature. However, he acknowledged the

danger that human activities may exacerbate the threat to corals both locally

and on a global scale. In the Arabian Gulf off the coast of Oman, Al-Jufaili et al.

(1999) documented significant impacts to coral reefs from natural and human

sources. Predation on corals by the starfish Acanthaster planci, storm damage,

coral disease, and temperature stress were the most prevalent natural

impacts, while fishing gear damage (primarily lost or abandoned gill nets)

caused significant damage on many reefs.

Messiha-Hanna and Ormond (1982) documented significant deterioration of

coral reefs in the Gulf of Suez area of the Red Sea. Although this reduction in

coral cover was ostensibly attributed to erosion by sea urchins (principally

Diadema setosum), the authors further linked the high numbers of urchins to

reduced numbers of their fish predators, which in turn was blamed partly on

fishing pressure. In addition, however, Messiha-Hanna and Ormond

suggested that the observed chronic oil pollution of the area was also

responsible for reduction in coral cover. They commented that regrowth and

reproduction would, under normal circumstances, mediate predatory

reduction in cover. However, the distribution of coral reef erosion suggested

that oil impaired those processes . Fishelson (1973) had similarly observed

that injured coral reefs do recover and regenerate; however, a necessary

condition for those to occur was the prevention/elimination of pollutant

stresses.

In his review of global and local threats to coral reefs, Wilkinson (1999) noted

that before 1998, direct and generally localized anthropogenic impacts
63

(increased sediment loading, pollution, over-exploitation) were regarded as

the major threat to coral reefs. However, in 1997-1998, the significance of

truly global coral reef threats was identified when unprecedented coral

bleaching occurred in pristine reef areas and modeling exercises showed that

increased ambient CO2 concentrations were expected to be increasingly

problematic.

Loya (1975) illustrated the interpretive dilemma in a coral reef system, the

northern Gulf of Eilat region of the Red Sea extensively studied by this

researcher over the years. Loya monitored two reef flats over the four-year

period 1969-1973—one in a nature reserve located near a refinery and several

other human activities, the other a control area removed from those

influences. Both areas supported rich and diverse coral reef communities. In

1970, an unexpectedly low tide exposed the reefs in both areas to very high

ambient temperatures for extended periods of time. The direct consequence

of these conditions was a mass mortality of about 90 percent of the

scleractinian corals in both the nature reserve and the control area. In the

subsequent years, distinctly different patterns of coral recolonization in the

two areas occurred. In 1973, the reef near the nature reserve was gray,

unattractive, and dominated by algal species. In contrast, the control reef had

rebounded in recolonization of corals to the point where numbers of

colonies exceeded those in 1969 before the low tide. While no significant

differences in community structure (number of species, number of colonies,

living coverage, diversity per transect) between the nature reserve and

control reef were found in 1969, all parameters were significantly higher at

the control in 1973.

Loya speculated as to the reasons for these distinct differences, and suggested

that oil spills, chronic oil pollution, phosphate eutrophication of a lagoon in

the reserve, thermal pollution from a desalinization plant, and coral breakage

from tourist activities all could have had potential roles in inhibiting

recolonization. Fishelson (1973) similarly attributed coral reef decline in the

area to proximity of the oil terminal (responsible, according to Fishelson, for

2-3 spills per month) and a phosphate loading operation. Unfortunately, there

was no way to determine the relative contribution of these and other

influences to the overall impact. Ray (1981) further noted that, while effects

on this reef were probably due to the high level of chronic oil pollution, it

would be difficult to extrapolate the findings generated there to other

locations for a given spill.

Loya’s work foreshadowed current concerns about incremental, cumulative,

detrimental changes occurring to coral reef systems worldwide. It is clear

that many coral ecosystems continue to be subjected to a range of stresses,

the most obvious being bleaching attributed to ambient temperature

increases. The additional stress imposed by an event such as an oil spill might

have a far greater impact on a weakened reef and reef community than the
64

single and isolated insult of a spill would otherwise be expected to represent.

There is a general recognition of the cumulative nature of environmental

stresses in corals in oil spill contingency planning, as shown by statements

such as this from Nansingh and Jurawan (1999) in an environmental sensitivity

mapping exercise in Trinidad:

Salybia Reef on the northeast coast of Trinidad exists at the limit of environmental tolerance of

corals due to seasonal low salinity and high turbidity conditions. This reef would be adversely

affected by the additional stress due to oil contamination.

A qualitatively different kind of synergistic spill effect consideration that

should at least be mentioned here is one we have explicitly avoided detailing

here in order to simplify the complex task of discussing oil impacts: the

potential synergistic increase in impact with the combination of oil and

chemical spill dispersants. The example we can cite here is the research of

Cook and Knap (1983), who found that, by themselves, exposure to crude oil

and a dispersant had no effect on coral photosynthesis. However, combining

the two significantly depressed total carbon fixation and significantly altered

into which chemical fraction the carbon was fixed. Although this was a

transient impact, it was one that occurred only when the two materials (oil

and dispersant) were combined. Other studies that comparatively examined

adverse effects to coral from oil alone and oil + chemical dispersant found

that combining the compounds increased toxicity. This, of course, carries

significant implications for spill response; but these are detailed elsewhere

(see, for example, the direct discussion of this subject in Hoff 2001).

SUMMARY

While a number of research efforts have been undertaken over the years to

elucidate the effects of oil on corals, extracting general lessons from the

resulting literature is difficult. Many, if not most, of the exposure methods

poorly document the concentrations of oil experienced by test corals. This

deficiency precludes comparing results across studies, and does not even offer

strong support for internally consistent exposures due to variability in how

oil mixes into water.

There is also the question of how realistically some research exposure

compare to spill exposures. That is, in the interest of obtaining a strong

response “signal,” some studies may have relied on oil exposure scenarios

that could be imagined only in the most extreme situations (which is not to

say, based on previous experiences, that they could not occur).

LABORATORY STUDIES

Over the last thirty years, many researchers have studied the effects of oil to

corals in the laboratory. Unfortunately, a large portion of the results can be

interpreted and extrapolated to oil spill scenarios only in a most general way,

primarily due to the way corals were exposed or to the way the oil exposure
65

was quantified. That is, our real-world expectation of oil exposure to reef

corals would be in the form of water-accommodated fractions of spilled

petroleum mixed into the water column, with the highest concentration

encountered early in the spill and steadily (probably rapidly) declining

concentrations over time. The available oil toxicity studies in corals rarely

come close to simulating this kind of exposure scenario, which renders the

application and extrapolation of results difficult and possibly inappropriate.

This does not mean that the body of research not portraying realistic spill

parameters is not useful, however— a great deal of information about the

range of effects resulting from oil exposure can be gleaned.

Some noteworthy laboratory studies based their experimental design on oil

exposures and exposure scenarios that could reasonably be expected during

actual spill events. These focused on oil exposure through wateraccommodated fraction at realistic levels that were measured and not merely

calculated. The exposures were pulsed or flow-through to approach

conditions during a spill incident and avoid complications from scale effects

and lack of circulation. Although many have commented that laboratory

results are difficult to extrapolate to field conditions, the studies that

incorporated the above considerations into their design and implementation

likely provide the most appropriately applicable results. The laboratory

studies that made good efforts to satisfy these conditions include:

Cook and Knap (1983)

Dodge et al. (1984)

Gardiner and Word (1997)

Harrison et al. (1990)

Knap et al. (1983)

Neff and Anderson (1981)

Peters et al. (1981)

Negri and Heyward (2000)

Based on what we and others have identified as some of the weak and strong

points from oil toxicity studies in coral, suggested laboratory parameters for

future studies are listed below. To the extent possible, we would

recommend using the experimental setup procedures and protocols of

CROSERF, the working group of the Chemical Response to Oil Spills

Ecological Effects Research Forum. These were developed through extensive

testing and discussions among an international group of toxicologists,

chemists, and physical scientists. These protocols are summarized in Singer

et al. (2001) and Singer et al. (in press). Some suggested parameters:

• Water-accommodated fractions as mechanism of exposure;

• At least three different oils: No. 2, No. 6, and at least one crude;

• Realistic exposure concentrations, measured by fluorescence or other

means, spanning a range of up to 50 ppm;
66

• Spiked exposure for comparison to constant concentration exposure and

to simulate spill conditions;

• Multiple species, with selection based on factors of particular interest

such as form (e.g., branching or massive), geography (e.g., Pacific/Oceania,

and Caribbean/Atlantic), reproductive strategy (brooder or spawner), or

mucus cover;

• Sensitive and multiple toxicity endpoints, such as molecular biomarkers,

as well as calculation of traditional acute endpoints such as LC50.

Of these, we believe that measurement of exposure concentrations is the

most critical, as it represents the most direct way to link laboratory

experiments to field or oil spill situations.

FIELD STUDIES

Although field studies ostensibly offer the best opportunity to study and

understand the effects of oil spills under realistic conditions, they are

uncommon in a coral reef setting. Rinkevich, Loya, and their colleagues have

studied and written about a heavily impacted spill area in the Red Sea, but

interpreting these results is complicated not only by the layering of spill

incidents with chronic oil pollution from refinery and terminal operations, but

also from a host of other human-induced stresses unrelated to oil. Perhaps

the best example of a field spill study is that of the 1986 Bahía Las Minas spill

in Panama, which had the good/bad fortune to have occurred near the

Smithsonian Tropical Research Station. The extensive series of studies

across that tropical system documented a number of short- and long-term

impacts attributed to the oil spill. The effects of the Bahía Las Minas spill are

discussed in (among others):

Burns and Knap (1989)

Guzmán et al. (1994)

Guzmán et al. (1991)

Guzmán and Holst (1993)

Guzmán and Jarvis (1996)

Jackson et al. (1989)

Keller and Jackson (1993)

The most carefully designed and monitored attempt to perform a

manipulative, large-scale field experiment with corals and oil was the 1984

TROPICS effort, sponsored by API. Intended to provide a degree of realism

within a relatively more controlled setting, TROPICS examined short- and

long-term effects of oil and dispersed oil to three common tropical habitats.

Interestingly, of the three habitats studied, the coral reefs were least affected

by exposure to oil alone. References for TROPICS are:

Ballou et al. (1987)

Dodge et al. (1995)
67

ACUTE EFFECTS

Many early studies of acute oil toxicity effects in coral involved what can only

be described as severe exposure conditions: submerging corals in marine

diesel for 30 minutes (Birkeland et al. 1976);holding corals under static

conditions in small (50- or 250-ml) containers with relatively large amounts

(1-4 ml) of oil (Reimer 1975); allowing crude oil to coat portions of coral

colonies exposed to the air (Johannes et al. 1972).

In the latter example, the extreme dosing had a basis in a potential spill

scenario, as the authors noted that some corals may be exposed during

periods of low tides in the Indo-Pacific region.

That any of the test corals survived these exposures for any length of time is

interesting, and in some cases even astonishing. It is notable that sometimes

a colony was not killed outright after a “dunking” in pure product, but

subsequently showed a steady decline in condition over a long (>100 days)

period, ending in death. This might lead us to question the definition of

“acute.” Another interpretive difficulty arises when conclusions of apparent

survival from high concentration exposure are compared to those of

Harrison et al. (1990), whose methods satisfied the criteria established above

for realism in a laboratory setting: Harrison et al. found that low-level

exposures (relative to the submersion in pure oil product that was

sometimes carried out) nearly completely disintegrated coral tissues after 48

hrs. While they had selected a coral species known for its sensitivity to

stress (A. formosa), these results taken at face value suggest that a brief

exposure (1-30 minutes) to extreme concentrations of oil is far less acutely

toxic than a longer (4-48 hrs.) exposure to low concentrations. Differences

in species’ tolerances are probably important here, with branching corals

among the most susceptible and massive corals more tolerant of oil

exposure.

The old notion that coral reefs do not suffer acute toxicity effects from oil

floating over them is probably incorrect. Certainly, direct coating increases

the severity of impact, but the water-accommodated fraction at

concentrations that could be encountered during a spill also appears capable

of causing rapid mortality (in addition to longer-term effects).

CHRONIC EFFECTS

In contrast to the situation with investigations into acute toxicity of oil to

corals, all researchers studying chronic effects documented sublethal changes

in exposed corals in some form. The diversity of impacts described in the

literature at least in part reflects an increasing degree of toxicological

sophistication and technical ability to document effects at suborganismal

levels. The literature also points to a realization that more subtle sublethal
68

manifestations of oil exposure may be most important in understanding how

a spill will affect a reef system.

Sublethal oil exposure appears to affect many normal biological functions.

From the available literature, it would seem that the function with the most

potential to adversely influence the survival dynamics of the corals themselves

would be those associated with reproduction and recruitment. A host of

studies have shown that oil reduces fecundity, decreases reproductive

success, and inhibits proper development of early life stages of corals. A spill

occurring at just the wrong time in a given area, at the peak of reproductive

activity, could cause immediate and long lasting harm to the communities of

corals themselves.

Oil also impairs two fundamental bioenergetic components for the entire

coral reef community: primary production by the zooxanthellae symbionts in

coral, and energy transfer via coral mucus. While some of the referenced

studies indicate that effects to these processes are transient and that corals

can recover from them in the absence of oil, circumstances of individual spills

will dictate whether these would be of concern to responders and resource

managers.

IMPLICATIONS FOR SPILL RESPONSE AND PLANNING

1. Oil is toxic to corals. Although Wilkinson (1999), in his review and

prediction of trends in coral reefs worldwide suggested that “...it is

unlikely that major oil spills near coral reefs will cause significant damage,”

most of the literature points to a potential for impact that cannot be

ignored. We can argue about how toxic oil is to corals and how that

toxicity is expressed, but it is clear that exposure to oil can adversely

affect corals. The difficult part is the quantification of exposure and effect

for the purposes of making (and justifying) the inevitable tradeoffs during a

spill. This exercise involves no easy answers, and the available science

offers only the most general guidance.

If we acknowledge the potential for adverse impact, the logical question

for responders to ask is, “ What level of exposure represents a threshold

for significant effects?”

• Direct contact between a living coral and oil, whether it is intertidally

or subtidally, is likely to result in serious pathologies or death of some

portion of the colony.

• Based on the admittedly limited literature in which exposure

concentrations were measured, a reasonable effects threshold in the

water column is 20 ppm. This is the concentration noted by Cook, Knap,

Dodge, and their colleagues as a level where sublethal impacts could be

elicited, as well as one representing a water concentration possible in a
69

spill scenario. Even at this relatively high water concentration, most of the

noted impacts were transient after a certain period of recovery in clean

water.

• Transient concentrations of oil in the water below 20 ppm are

probably not likely to result in lasting harm to a coral reef. The key word

here, outside of “probably,” is “transient.” This implies that such a

concentration would be sustained and experienced for only a short time.

The situation where such a level is a chronic parameter, where there is a

continuing source, may result in more serious pathological effects to

exposed coral reef communities.

• It would be reasonable to expect that much lower concentrations of

oil in water could harm larvae of coral or impair normal reproductive

processes. The work of Negri and Heyward, which at least measured

concentrations of the stock solution used in preparing dilutions, identified

a threshold for fertilization inhibition at 0.165 ppm.

2. Time of year is critical. A spill of a given size of a given oil in a given

area may have dramatically different impacts depending on the time of year

in which it occurs. While this is true of any environment anywhere in the

world, it is especially true for coral reefs, where reproductive and early

life stages are known to be particularly sensitive to oil. In other words, if

we know who is reproducing when, it takes us a long way toward

determining whether the spill has an enhanced potential for injury to the

corals. Appendix C is intended to help define periods of increased

vulnerability.

In many areas of the world, spring and summer are peak reproductive

periods. This is reflected in Appendix C. This seasonal timing for

spawning has been noted especially in coral reefs like the Great Barrier

Reef, where the synchrony of timing becomes even more narrowly

focused to specific lunar phases and more broadly defined to include a

wide segment of the reef community beyond corals. In such a system, an

ill-timed spill (which is not to imply there is such a thing as a well-timed

spill) has the potential to wipe out a sizable portion of a given year’s

recruitment for many community members.

3. Expert knowledge should be used. Coral experts who have

knowledge of the reefs of concern should play a key role in shaping a

response strategy. For example, local biologists may be able to tell

whether a threatened area is dominated by branching corals, thought to be

sensitive to oil, or massive corals, thought to be more tolerant. They

may know about life histories, a key consideration as suggested above.

They should have information about the presence of threatened or

especially sensitive reef community members.
70

Resource managers in particular will be able to provide useful and relevant

information about portions of a reef community that may be experiencing

greater stress from (for example) a recent grounding or hurricane

damage. In this way, such experts can help to identify areas for increased

protection or areas where such efforts may not be worth the effort.

4. Cumulative impacts complicate things. Everything that we know

about oil and corals may be moot if the reef in question is under serious

stress from other sources before the spill. Currently, concerns about

coral reef deterioration are nearly universal. Warming of the oceans has

been identified as a key factor in widespread coral bleaching events;

physical destruction from recreational boating or fishing activity has been

locally significant; human pollution and land use policies have contributed

to degradation. It is possible that an oil spill in any area subjected to

substantial but unrelated stress may represent a synergistic “tipping

point,” an impact that ordinarily would not cause significant damage, but

that against the background of other stresses causes a rapid cascade of

seemingly irreversible decline in the reef system.

New tools that could help us determine the pre-existing status of a coral reef

and also isolate effects of oil spills may be imminent. For example, Downs et

al. (2000) describe a molecular biomarker system capable of discriminating

among different sources of stress to identify (and even predict) corals at risk

from bleaching. Their approach assays specific parameters of coral cellular

function to gauge degree of stress; each parameter was chosen because it

reflects specific cellular physiological functions. If this approach is validated

and can be readily adapted to the field, it could provide an excellent way to

ascertain status of a coral community and evaluate relative sources of overall

stress in an impacted area.

Even with the promise of new technologies, spill responders will continue to

labor under the burden of incomplete and not entirely relevant information.

Despite any common ground that may exist from previous incidents, each

spill represents a new and unique set of circumstances. The studies we have

summarized here provide a background of research against which we can

evaluate alternatives and extrapolate effects. There will, however, always be

some degree of judgment call associated with the exercise.
71

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81

APPENDIX A

GLOSSARY/ACRONYMS

API: American Petroleum Institute

arborescent: like a tree in growth, structure, or appearance.

aromatic hydrocarbon: a class of unsaturated hydrocarbons characterized by

rings containing six carbon atoms and three conjugated double bonds.

broadcasting: method of reproduction utilized by some corals in which

gametes are released into the water column

brooding: method of reproduction in some corals in which reproduction

occurs in place.

bunker oils: viscous fuel oils (usually designated by letters B or C, or

numbers 5 or 6) used primarily in marine and industrial boilers.

coenosarc: the hollow stem and living basal parts of colonial hydroids, which

houses a continuous gastrovascular cavity.

depuration: passive or diffusive loss of contaminants from an organism.

dioecious: having the male and female reproductive organs in separate

individuals (most animal species are dioecious, as are some plants, such as

asparagus).

dispersant; a chemical formulation containing surface active agents and/or

solvents that lower the interfacial tension between oil and water and enable

the oil film to break up more easily under natural wave action or mechanical

agitation.

dispersion: the distribution of spilled oil into the upper layers of the water

column by natural wave action or by application of chemical dispersants.

elimination: combined processes of metabolism, excretion, and diffusive loss

of contaminants from an organism.

FAA: Federal Aviation Administration

gas chromatography: analytical method used to aid identification of oil

constituents in which a mixture of volatile substances (e.g., oil) is carried by

an inert gas through a tube containing a non-volatile liquid supported on an

inert porous solid. Movement of the various components is selectively

retarded, thus permitting their separation and subsequent identification.
82

GC-FID: gas chromatography/flame ionization detector

GC/MS: gas chromatography/mass spectrometry

GLC/FID: gas-liquid chromatography/flame ionization detector

gonochoric: animals having separate sexes.

hermaphroditic: an animal possessing both male and female functional

reproductive organs, such as the earthworm; or a unisexual animal having

male and female gonads as an aberration.

hermatypic: reef-building

hormesis: enhancement of a physiological process, also termed Arndt-Schult

effect, in response to stress.

hydrocarbons: organic compounds composed only of the elements carbon

and hydrogen; principal constituents of crude oils, natural gas, and refined

petroleum products.

LD50: concentration of a substance that causes death in 50 percent of a test

population

massive: when referring to coral types, describes a skeleton formed as a

solid block rather than being branched or plate-like.

MSRC: Marine Spill Response Corporation

octocoral: one of two subclasses of corals, colonial anthozoan coelenterates

with eight-branched tentacles, including soft corals, horny corals, and sea

pens.

planula: the ciliated, free-swimming larva of a coelenterate.

ppb: parts per billion

ppm: parts per million

protandrous: sequential hermaphroditism in which an organism changes sex

from male to female.

protogynous: sequential hermaphroditism in which an organism changes sex

from female to male.

RD50: concentration of a substance that results in a given response in 50

percent of a test population
83

scleractinian: any of the corals of the order Scleractinia; this still-abundant

order first appeared in the Triassic and was the first to replace the tabulate

and rugose corals, which had disappeared at the end of the Permian.

sclerochronology: the study of scleractinian coral growth rings

WAF: water-accommodated fraction, that portion of a substance dissolved

or suspended in water.

weathering: the alteration of the physical and chemical properties of spilled

oil through a series of natural biological, physical, and chemical processes

beginning when the spill occurs and continuing as long as the oil remains in the

environment; contributing processes include spreading, evaporation,

dissolution, dispersion, photochemical oxidation, emulsification, microbial

degradation, adsorption to suspended particulate material, stranding, or

sedimentation.

WSF: water-soluble fraction, that portion of a substance which truly

dissolves in water.

zooxanthellae: plantlike flagellate protozoans in the order Dinoflagellida,

photosynthesizing symbiotes inside the cells of sponges, corals, and others.
84

APPENDIX B

CORAL SPECIES CITATION LIST

Cross-reference of coral species mentioned in referenced papers

Acropora cervicornia

Neff and Anderson (1981); Ballou et al. (1987)

Acropora elsyii

Neff et al. (1998)

Acropora formosa

Craik (1991); Harriott (1993); Harrison et al. (1990)

Acropora millepora

Negri and Heyward (2000)

Acropora palmata

Neff and Anderson (1981); Bak (1987)

Acropora spp.

Spooner (1970); LeGore et al. (1989)

Agaricia agaricites

Lewis (1971)

Agaricia tenuifolia

Ballou et al. (1987); Burns and Knap (1989); Dodge et al. (1995)

Diploria clivosa

Jackson et al. (1989); Guzmán et al. (1994)

Diploria strigosa

Bak (1987); Knap et al. (1982); Cook and Knap (1983); Dodge et al. (1984);

Guzmán et al. (1994)

Favia fragrum

Lewis (1971); Neff and Anderson (1981); Kennedy et al. (1992)

Favia speciosa

Grant (1970)

Fungia scutaria

Johannes (1975)

Goniopora sp.

LeGore (1989)
85

Heteroxenia fuscescense

Cohen et al. (1977); Kushmaro et al. (1996); Epstein et al. (2000)

Madracis asperula

Lewis (1971)

Madracis decatis

Neff and Anderson (1981)

Madracis mirabilis

Elgershuizen and deKruijf (1976)

Manicina areolata

Peters et al. (1981)

Millepora sp.

Neff and Anderson (1981)

Montastrea annularis

Neff and Anderson (1981); Bak (1987); Ballou et al. (1987); Kennedy et al.

(1992)

Montipora verrucosa

Johannes (1975)

Oculina diffusa

Neff and Anderson (1981)

Pavona gigantea

Birkeland et al. (1976)

Platigyra sp.

Mitchell and Chet (1975); LeGore et al. (1989)

Pocillopora cf. damicornis

Birkeland et al. (1976); Te (1991); Harriott (1993)

Porites spp.

Jackson et al. (1989); Lough and Barnes (1997)

Porites astreoides

Rützler and Sterrer (1970); Jackson et al. (1989); Guzmán et al. (1994);

Ruesink (1997)

Porites compressa

Johannes (1975)

Porites furcata
86

Rützler and Sterrer (1970); Birkeland et al. (1976)

Porites lutea

Readman et al. (1996)

Porites porites

Lewis (1971); Ballou et al. (1987); Dodge et al. (1995)

Porites sp.

LeGore (1989)

Psammocora stellata

Birkeland et al. (1976)

Siderastrea radians

Rützler and Sterrer (1970)

Siderastrea siderea

Burns and Knap (1989); Jackson et al. (1989); Guzmán and Holst (1993);

Guzmán et al. (1994); Guzmán and Jarvis (1996); Ruesink (1997)

Stylophora pistillata

Rinkevich and Loya (1977); Loya and Rinkevich (1979); Rinkevich and Loya

(1979); Rinkevich and Loya (1983); Epstein et al. (2000)

Tubastrea aurea

Brey et al. (1995)
87

APPENDIX C

REPRODUCTIVE TYPE AND TIMING, BY REGION

(Adapted from Richmond and Hunter 1990; and Kenyon 1992)

These figures are intended to provide a quick reference about reproductive

type (brood or spawn) and timing over the year for coral species for which

information is available. Source information was extracted from tables in

Richmond and Hunter (1990) and, for Acropora species in Hawaii, from

Kenyon (1992). Refer to these papers for additional and more detailed data,

as well as original data sources.

The information is organized by region (Caribbean, Great Barrier Reef,

Hawaii, Okinawa, Central Pacific, and Red Sea). Coral species for which

reproductive information was available are listed down the vertical axis, and

months of the year are listed across the horizontal axis. If a species is known

to spawn (i.e., broadcast zygotes into the water column) it is shown in red; if

a species broods (i.e., retains gametes within a colony) it is shown in blue. If

reproductive strategy is unknown, it is shown in gray. A white bar reflects

that the species was reported to be possibly sterile. A dotted line indicates

that timing of reproduction is unknown.

The graphic presentation of data is an easy way to identify periods of

increased sensitivity or susceptibility for the coral species of a given region.

For example, in examining the ample information for the Great Barrier Reef,

it becomes apparent that November would be an especially bad time of the

year to have an oil spill. A responder or resource manager may choose to

structure a response or cleanup strategy around this fact by (for example)

minimizing activities that could increase levels of oil in the upper portions of

the water column where coral gametes and larvae would be expected.