OIL SPILL SCIENCE chapter 27 – effects of oil in the environment

OIL SPILL SCIENCE chapter 27 – effects of oil in the environment OIL SPILL SCIENCE chapter 27 – effects of oil in the environment OIL SPILL SCIENCE chapter 27 – effects of oil in the environment OIL SPILL SCIENCE chapter 27 – effects of oil in the environment OIL SPILL SCIENCE chapter 27 – effects of oil in the environment OIL SPILL SCIENCE chapter 27 – effects of oil in the environment OIL SPILL SCIENCE chapter 27 – effects of oil in the environment

Chapter 27 Effects of Oil in the Environment Gary Shigenaka Chapter Outline 27.1 Introduction 27.2 Some Definitions 27.3 Size Matters: Seeps vs Spills 27.4 An “Equation” to Convey Toxic Impact 27.5 Route of Exposure: The Anthrax Example 27.6 Route of Exposure: Oil 27.7 Oil Chemistry, Physical Behavior, and Oil Effects 985 987 989 991 999 1000 27.8 Freshwater/Saltwater Differences 27.9 Tropical Environments 27.10 Arctic Environments 27.11 Ecological Effects of Oil Spills 27.12 The Future of Oil Effects Science 27.13 Summary and Conclusions 1008 1010 1013 1014 1017 1019 1003 27.1 INTRODUCTION Doull and Bruce write that “Toxicology.is both a science and an art,” with the science defined as the observational or empirical phase, and the art as the predictive phase, with the linkage between the two represented by the need to apply the former to accomplish the latter.1 In this sense, assessment of oil spill effects provides an excellent, sometimes befuddling, and often frustrating example: we empirically observe the behavior and effects of oil in the laboratory, and we can record impacts from an actual oil spill when it occursdbut linking the pieces, predicting the effects of a given release of a given oil potentially impacting a given set of resources in a given area, may be less of an art than it is magic.or wishful thinking This is to say: we haven’t quite figured it all out yet But, we seem to be getting closer A common perception of the effects of oil in the environment is captured in the evocative photographs and footage of oiled wildlife struggling after Oil Spill Science and Technology DOI: 10.1016/B978-1-85617-943-0.10027-9 Copyright Ó 2011 Elsevier Inc All rights reserved 985 986 PART | X Effects of Oil in the Environment exposure to a spill While the impacts represented by this kind of outcome are only a few of the many possible, they are visually compelling, memorable, and by default assumed by many to be diagnostic for what occurs when oil intersects with the environment With these kinds of images burned into the collective consciousness and id, nearly any elementary school student or viewer of the evening news can tell us, with some certainty, that oil is indeed harmful The recent (2010) Deepwater Horizon oil spill in the Gulf of Mexico, and its attendant media coverage, have done little to dispel the notion that these events are ecological and human disasters of the first order The early images of bright red oil emulsions stretching for miles on the water, thousands of response and recovery vessels near the accident site, massive applications of chemical dispersants, plumes of smoke from burning of oil slicks, the inevitable photographs of oiled pelicans and sea turtles, and stories about impacted fishing communities and local and regional economies only serve to underscore the perception that oil spill IMPACTS are profound and far-reaching Similarly, the scientific literature contains countless studies that document toxicity of petroleum products and their chemical constituents to virtually the entire spectra of plants and animals But not every oil spill is an environmental catastrophedand even the same spill incident variably affects different organisms in different ways, at a given moment and over time The empirical view from 40,000 feet suggests that generalizations about impacts may not be appropriatedand we begin to sense the challenges of understanding the effects of oil Some of these challenges have been articulated by others undertaking the task of rendering at least a portion of the oil impacts universe into something that we can understand: l l l l Determining the effects of oil is complex, and generalizing about effects is difficult One must remember that specific impacts are very species and situation dependent.2 Because many physical and biological processes in the marine and coastal environment are poorly understood, it is difficult for scientists to measure the full impacts of an oil spill, and sometimes the results appear contradictory.3 Oil spills will have different environmental effects.the environmental effects will depend on factors such as type of oil, different oceanographic conditions, latitude, season, and type of ecosystem.this complicates extrapolation of data in even the most general terms.4 Many spill impacts have been documented in the scientific and technical literature, and although not all the effects of oil pollution are completely understood, an indication of the likely scale and duration of damage can usually be deduced from the information available However, it can be difficult to present a balanced view of the realities of spill effects.the simple reality is that sometimes significant damage occurs, sometimes not.5 Chapter | 27 Effects of Oil in the Environment l 987 Oil can kill marine organisms, reduce their fitness through sublethal effects, and disrupt the structure and function of marine communities and ecosystems While such effects have been unambiguously established in laboratory studies.and after well-studied spills determining the subtler effects on populations, communities, and ecosystems.poses significant scientific challenges.6 Petroleum is, of course, a natural material that is extracted like other minerals and then processed and refined into thousands of products applied to a myriad of general and specialized uses Oil spills are one of the unfortunate consequences of accidents that occur during the extraction, production, or transportation processes, or during end uses However, oil is also released naturally into both terrestrial and marine environments through seeps, where oil deposits close to the surface of the soil or sediment are exposed Rather than reflect severe biological impacts from this chronic localized exposure, these natural oil seep areas can be remarkable in their lack of apparent effects That is, despite the presence of what amounts to be large, continuous oil spills, oil seep areas not show impacts commensurate with our perceptions of oil as a poison and the results of research that confirm those perceptions How we reconcile these disparate notions and observations in order to understand the effects of oil in the environment? In this chapter, we will discuss the characteristics of the substances we consider to be “oil” and describe how these form the basis for a complex formula to be solved in order to understand how oil affects organisms exposed during oil spills We will summarize the toxicology and research studies that have helped us to understand if and how oil is harmful Finally, we will consider the implications for oil spill response 27.2 SOME DEFINITIONS The derivation of the word, “oil” dates to 13th-century Middle English (oile), and stems from Latin (oleum) and Greek (elaion) terms relating, not surprisingly, to olive oil and olives The official Merriam-Webster definition for oil is “any of numerous unctuous combustible substances that are liquid or can be liquefied easily on warming, are soluble in ether but not in water, and leave a greasy stain on paper or cloth.” The particular oils with which we are concerned for the purposes of this book are those derived from petroleum Referring again to Merriam-Webster, this takes us to a more focused definition: “an oily flammable bituminous liquid that may vary from almost colorless to black, occurs in many places in the upper strata of the earth, is a complex mixture of hydrocarbons with small amounts of other substances, and is prepared for use as gasoline, naphtha, or other products by various refining processes.” 988 PART | X Effects of Oil in the Environment A part of this lengthy definitiond“a complex mixture of hydrocarbons”d reflects one of the key concepts relevant to the environmental impacts of petroleum oil spills: oil, specifically petroleum oil, is not a singular substance that is the same from place-to-place, time-to-time, and, for our purposes, from spill-to-spill As we shall learn, this fact immensely complicates our task of understanding the behavior and effects of oil Toxicity is another concept about which all of us have some intuitive understanding A simple but broadly applicable definition for toxicity is “the degree to which a substance is able to damage an exposed organism.” In the case of oil, however, the simplicity of this definition begins to elude us as we dissect it into its component parts and consider it in the context of petroleum; we can use it to preview the actual difficulty of discussing the toxicity of oil For example: the degree to which a substance is able to damage an exposed organism As we noted in the preceding definition, the oil we are considering is not a single substance, but a complex mixture of many substances, or chemicals This means that our assessment of oil toxicity begins with as many oil constituents or constituent groups as we care to evaluate .the degree to which a substance is able to damage an exposed organism What we mean by the term, “damage?” Does this means only a lethal endpoint? Or does it include sublethal injury from which an organism might recover? Does cellular injury that we cannot link to some observable impairment constitute damage? What about behavioral shifts resulting from exposure? Or shifts in community structure? Given the rather dynamic and elusive elixir that we suspect petroleum to be, we can begin to anticipate the many permutations of impact that will result if we consider multiple substances and multiple endpoints for damage .the degree to which a substance is able to damage an exposed organism The definition infers that exposure is a precondition for damage If a poisonous material does not come into contact with an organism of concern, is it still toxic? This may sound a little bit like the old philosophical riddle, “If a tree falls in the woods and nobody hears it, does it make a sound?” But this is a highly relevant question from the perspective of spill response, because if we accept that reducing exposure reduces impact, we can attempt to implement measures for reducing or preventing oil from coming into contact with a resource of concern .the degree to which a substance is able to damage an exposed organism It is a fact of toxicology that there are differences in the way a given toxin or toxic mixture affects different organisms and even different life stages of the same organism Therefore, consideration of multiple organisms or life Chapter | 27 Effects of Oil in the Environment 989 stages in an assessment of oil effect complicates our already challenging task by an additional possibly daunting factor We will use the definitions above as a template for discussing the basics of oil effects in the environment and will expand on the challenges they represent to us when we assess and respond to an oil spill 27.3 SIZE MATTERS: SEEPS VS SPILLS In its raw form, oil is a natural material that can readily be found, in many parts of the world, above ground or on the water, and is quite visible The National Research Council estimated that 45% of the oil entering the world’s oceans derives from natural seepage from geologic formations, and Hoefler counted 200 natural underwater oil seeps that have been identified around the world.5,7 One of the best-known of these areas lies offshore from Santa Barbara, California, near Coal Oil Point These seeps release 20e25 tons of oil each day, ultimately resulting in a degree of nearshore sediment oiling equivalent to 8e80 Exxon Valdez-size spills, as well as countless tarballs on the beaches of the central California coast.8 By any measure, this is a considerable amount of oil in a relatively small portion of the marine environment This same area is also known as the site of the first major oil spill disaster in U.S history, the Santa Barbara spill of 1969 However, the seeps and the iconic historical spill are only marginally related That is, although the oil spilled in 1969 derived from the same source that feeds the seeps (an oil-rich geologic feature called the Venture Avenue Anticline), the seeps themselves were not responsible for the spill Rather, it was a blowout at a production platform tapped into the submarine oil reservoir: uncompensated pressure increases in a 3500-foot well drilled under Union Oil Platform Alpha split the well casing and then fractured the seafloor around it, allowing oil to leak uncontrollably into the water column directly from the reservoir By the time the source of the spill had been contained (11 days later), approximately million gallons of oil had been released.9 News reports showed beaches with oil pooled as deeply as inches, along with oiled, dead seabirds and marine mammals Photographs, film footage, and written accounts of these and other spill-related impacts not only stoked public resentment against oil companies, they also played an important role in fostering the beginnings of the American environmental movement that culminated in the first Earth Day celebration and the passage of landmark U.S legislation to strengthen environmental protection As noted by U.S President Richard Nixon, “The Santa Barbara incident has frankly touched the conscience of the American people.” The Santa Barbara oil seeps and the 1969 oil spill are extreme examples of the same-source crude oil released into the same marine environment, but resulting in very different perceived and documented impacts The oil seeps 990 PART | X Effects of Oil in the Environment have been and continue to be generally considered as an inconvenience or nuisance, requiring tar to be cleaned off the feet of beachgoers and blankets; the Santa Barbara spill, on the other hand, was a seminal event in U.S environmental history whose impacts were seen as devastating and ultimately farreaching The continuous inputs from the Coal Oil Point seeps and the lack of adverse environmental impact related to them suggest that the marine environment can tolerate some level of exposure to oil; however, the dramatic impacts from the Santa Barbara spill illustrate that an effects threshold can be and was exceeded How we account for the range of impacts (or nonimpacts), and how can we apply this insight to other oil spill situations? What are the lessons for oil spill response? More narrowly focused studies of the biology of oil seeps have revealed relatively moderate effects attributable to oil exposure in this setting For example, Helix summarized the studies of benthic communities around the seeps and did not find the areas to be substantially affected.10 In fact, proximity to natural oil and gas seeps actually increased overall productivity and enhanced fecundity in species like copepods, which are generally considered to be sensitive to hydrocarbon exposure Spies et al studied benthic organisms as well as fish around the California seeps and found few indications of adverse impactdalthough fish sampled near the oil sources showed physiological evidence of aromatic hydrocarbon exposure (i.e., enzyme activation) and had higher incidences of gill and liver lesions.11,12 In this case, documented oil exposure did not translate into documented oil effect Helix attributed the modest incidence of adverse effects to a number of factors: l l l l Seeps are patchy in distribution, and amounts released are quite variable The oil to which communities are exposed varies in degree of “freshness,” which substantially influences toxicity Different biological communities have differing tolerances to the different levels of exposure Some organisms are capable of adapting to the presence of oil, either by accommodating or simply avoiding accumulations of oil We can make the same kinds of analytical observations for human-caused oil spills to suggest why more adverse impacts may occur, even when the same oil source as relatively benign seeps is involved: l l Oil spills are not uniform in distribution of product released (i.e., patchy), so the amounts to which organisms are exposed can vary widely Spilled oils vary widely in chemical composition, from highly refined fuels to unrefined crude oils and remnants of the refining process Adding to this complexity is the fact that spilled oil changes, or weathers, once it is released into the environment, and so the same oil days or weeks after a spill occurs is likely to differ substantially from the fresh oil initially released It Chapter | 27 Effects of Oil in the Environment l l 991 is essentially a different kind of oil spill, even with a single original source oil These differences considerably affect the native toxicity of the product, as well as our assessment of that toxicity Different biological communities have differing tolerances to the different products and different levels of exposure In an oil spill situation, the sheer volume of oil released into the environment over a relatively short period of time tends to overwhelm any inherent capability of the affected environment (also referred to as “net assimilative capacity” by Overton et al.13) to tolerate or accommodate exposure to the oil In the seep versus Santa Barbara spill example, all of the considerations played a role in very different effects profiles However, the differences in volumes spilled over time probably were the most significant Although 20-25 tons of oil per day released from seeps is a considerable amount of oild equivalent to around 7000 gallons per daydthe total for an 11-day period (the length of the uncontrolled Santa Barbara spill) would amount to a maximum of around 85,000 gallons This is far less oil than the estimated million gallons released by the Platform Alpha blowout Based on the empirical qualitative and quantitative information we have at our disposal, we can make some crude assignments of impact for the ongoing Santa Barbara seep release and the Platform Alpha release: 85,000 gallons/11 days (seep release) ¼ not so bad; 3,000,000 gallons/11 days (Platform Alpha) ¼ bad It should be abundantly apparent that at this scale, the impact assessment is not quantum mechanics, nor are the results transferable to stone tablets It could also be argued that a metric of “bad” overstates the broader population or ecological impact represented by the hundreds to thousands of bird and marine mammal mortalitiesdalthough the social/political/cultural/historical significance of the 1969 spill cannot be denied Also, less debatable is the dubious wisdom of then-Union Oil President Fred L Hartley’s stated opinion (Clarke and Hemphill9) concerning the singular lens through which he interpreted the impacts of the Santa Barbara spill: “I don’t like to call it a disaster, because there has been no loss of human life I am amazed at the publicity for the loss of a few birds.” 27.4 AN “EQUATION” TO CONVEY TOXIC IMPACT Our task here does not include factoring in the cultural or social contexts of oil spills in determining overall effect or impact (though we should note that completely ignoring those other contexts would be very foolish indeeddthey simply are to be contemplated elsewhere) That reprieve, however, does not necessarily simplify the challenge of assessing or predicting our more narrowly construed biological impacts It remains a daunting task 992 PART | X Effects of Oil in the Environment How, then, can we begin to sort through the facts of what is known about oil toxicity and the documented effects of a given spill event to make some sense of it all, to extract some pearls of wisdom to take with us to the next oil spill response? First of all, although we suggested above that size (of a release) matters, it is useful to think beyond only bulk amounts of oil introduced into a habitat of concern when assessing effects of that oil Yes, the amount of oil inflicted on biological communities is important But additional considerations enter into the calculus of impact The amount of oil is equivalent to the dose But the oil also has a unique toxicity signature that results from the complex chemistry we have discussed Finally, the extent and the characteristics of exposure to organisms and communities of concern is itself the result of a complex series of physical interactions dependent on the chemistry of the oil, the physics of its interaction with receiving waters, and the dynamics of how it is moved and distributed in the environment We can reduce this to a deceptively simple “equation”: Oil Impact ¼ Dose  Toxicity  Exposure or some function thereof This can be applied to specific oils and to individual organisms as well as to portray potential overall effect of entire spills We can work through several permutations of this function, with information from actual incidents to understand how it works A few examples follow Case 1: High Dose  High Toxicity  High Exposure (North Cape, 1996) Dose ¼ 828,000 gallons, high dose Toxicity ¼ Home heating oil, similar to diesel, higher acute toxicity Exposure ¼ Storm conditions in nearshore zone of Rhode Island mixed oil throughout water column Impact ¼ High, widespread highly visible mortalities of benthic organisms, some with high intrinsic and cultural value (lobsters) Case 2: High Dose  Medium Toxicity  Low Exposure (Odyssey, 1988) Dose ¼ 40 million gallons, very high Toxicity ¼ Crude oil, medium toxicity Exposure ¼ Low, tanker broke apart 900 miles off the coast of Newfoundland Impact ¼ Low, limited landfall for spilled oil Case 3: High Dose  Low Toxicity  Low Exposure (Barge DM932, 2008) Dose ¼ 420,000 gallons, medium Toxicity ¼ #6 fuel oil (“bunker”), lower acute toxicity but higher density and viscosity, potential for submergence and wildlife fouling impacts Exposure ¼ Low, despite downstream transport and stranding along 200 miles of Mississippi River banks Impact ¼ Extensive shoreline fouling, some recreational use impacts in New Orleans, minimal resource impacts Case 4: Low Dose  Medium Toxicity  Low Exposure (Cosco Busan, 2007) Chapter | 27 Effects of Oil in the Environment 993 Dose ¼ 53,000 gallons, low Toxicity ¼ Intermediate fuel oil, medium acute toxicity Exposure ¼ Low Impact ¼ High; heavily populated urban area, impacted recreational uses; Congressional hearings The difficulties and variability inherent in interpreting the biological impacts of oil spills are not a recent epiphany for researchers In 1974, Anderson et al commented on the tremendous variability of documented damages from larger spills to that time.14 They attributed the range of impacts to differences in environmental and geographic conditions at spill sites, and to differences in the spilled oils themselves In the preceding examples, we have shown only a few different permutations of the many (3   ¼ 27, if we accept that there are three qualitative levels of low, medium, and high for each of the three components of the impact equation) If we choose to refine the levels to include more nuance beyond high, medium, and low, then correspondingly more combinations are generated The point of this is the impact and the factors that enter into generating it There are many paths to the same destinationdwhich may sound like cheap philosophy, but it simply indicates that very different inputs into the impact equation can generate similar results Or the flip side of the mixed metaphorical coin is that the presence or absence of one or more factors can amplify or negate another factor Finally, it is impossible to anticipate and account for everything, as in the Cosco Busan example The metrics of our simple equation alone would have calculated that this spill would be minor in its impact, but public opinion, media coverage, and political interest elevated perceived impact to a much higher level The dose/toxicity/exposure equation incorporates the information inputs we consider during spill response, that is, how much spilled, what spilled, what can be done to protect valued resources? Of those three considerations in a response, two are relatively easily addressed: how much spilled (dose), and what can we to contain/divert/collect the spilled material (exposure)? The most difficult piece for us to determine, all other things being equal, is the “what spilled question,” along with its implications A narrower focus on impacts leads us to pose more questions about details and brings to the fore the questions of what the composition of the spilled material is and what is its toxicity In the case of oil products, the questions can be slightly rephrased to ask, how we expect the oil to harm? For a spill responder, the answer to that question then doubles back to considerations of oil behavior, exposure, and the differences implicit in routes of exposure The petroleum industry often characterizes crude oils according to their geographic source location, for example, Alaska North Slope crude However, this designation by itself does not provide any insight into fate and effects if the oil is spilled, and it is not very useful for response personnel That is, oil toxicity, 994 PART | X Effects of Oil in the Environment physical state, and the changes that occur with time and weathering are not conveyed or distinguished by geographic source names The U.S Environmental Protection Agency (EPA) uses the physical characteristics of petroleum oils as a way to consider the many types of oils from a response-oriented perspective; that is, how will the oil behave in the environment, and how will exposed organisms respond? The four U.S EPA categories are defined as:15 Light, Volatile Oils These oils are highly fluid, often clear, spread rapidly on solid or water surfaces, have a strong odor, a high evaporation rate, and are usually flammable They penetrate porous surfaces, such as dirt and sand, and may be persistent in such a matrix They not tend to adhere to surfaces; flushing with water generally removes them Light, volatile oils may be highly toxic to humans, fish, and other biota Most refined products and many of the highest quality light crudes can be included in this class Nonsticky Oils These oils have a waxy or oily feel They are less toxic and adhere more firmly to surfaces than light, volatile oils, although they can be removed from surfaces by vigorous flushing As temperatures rise, their tendency to penetrate porous substrates increases and they can be persistent Evaporation of volatiles may lead to a heavier and more persistent residue oil Medium-to-heavy paraffin-based oils fall into this class Heavy, Sticky Oils These oils are characteristically viscous, sticky or tarry, and brown or black Flushing with water will not readily remove this material from surfaces, but the oil does not readily penetrate porous surfaces The density of heavy, sticky oils may be near that of water, and they often sink Weathering or evaporation of volatiles may produce solid or tarry nonfluid oil Toxicity is low, but wildlife can be smothered or drowned when contaminated This class includes residual fuel oils and medium to heavy crudes Nonfluid Oils These oils are relatively nontoxic, not penetrate porous substrates, and are usually black or dark brown in color When heated, nonfluid oils may melt and coat surfaces that become very difficult to clean Residual oils, heavy crude oils, some high-paraffin oils, and some weathered oils fall into this class During an oil spill, these classifications are dynamic and may change for a given product released into the environment, dependent on the effects of weathering or more transient changes such as ambient temperature As we have noted, these influence the state and behavior of crude oil and refined petroleum products For example, as volatiles evaporate from a nonsticky oil, it may become a heavier product with different physical characteristics If a significant temperature drop occurs (e.g., at night), a heavy, but still fluid, oil may solidify Upon warming, however, it may revert back to its original state A general rule of thumb for oil spill responders has long been that the refined fractions of crude oil, like gasoline or jet fuels, were the most toxic of 1010 PART | X Effects of Oil in the Environment generalisations with any confidence It is hoped that future work will overcome many of the fundamental flaws and gaps in our understanding.” For biological and ecological effects in fresh water, Trett et al noted that while numerous studies exist, effort has not been evenly focused across taxonomic groups.47 Further, that while links between number of aromatic rings and degree of alkylation to increasing toxicity were documented, actual results of toxicity tests varied widely even among closely related species Finally, they commented that in contrast to toxicity studies, relatively little work on mutagenicity and carcinogenicity in freshwater species had taken place In other words, the interpretive framework for oil effects in the freshwater environment is just as frustrating as it is for the marine environment Amphibians present an interesting case, unique to fresh water, in that their life cycles are so intimately associated with and dependent on the aquatic habitat Widely publicized declines of amphibian populations worldwide have prompted investigations into potential causes Beyond the obvious potential impacts of environmental degradation and contamination, investigators have also assessed synergistic interactions Little et al studied photoenhanced toxicity (more detailed discussion follows below) of water-soluble fractions of weathered petroleum.48 They found that solar radiation substantially increased toxicity of the weathered oil fraction Beyond the synergistic potential of light and oil to increase toxicity to amphibians, the fundamental reliance of this class of animals on clean water would present a concern during spills in freshwater habitats It has long been known (Jorgensen49 cites a study by Spallanzani in 1803) that amphibians satisfy a significant portion of their respiratory requirements cutaneously, that is, by breathing through their skin Any interference with this ability, as could be expected in oil contact by either/both physical fouling and PAH inhibition of proper cell function, would impair the fitness of the exposed animal As there is little that could be done for extensively oiled animals in a spill situation, minimization of exposure would be a priority for resource protection 27.9 TROPICAL ENVIRONMENTS For our brief foray into oil toxicity, it is necessary to reduce distinctly complex habitats into simpler distinguishing characteristics and then refer interested readers to the ample literature on environments of concern It is a necessary concession; otherwise, this single chapter would overwhelm the rest of the book and diminish the lucrative payments that the other authors expect to receive for their contributions (which we believe will be calculated by the editor as a percentage of total book weight basis) Tropical habitats, for example, can be thought of as having distinct features, such as warm temperatures, exceptional water clarity, and potentially highenergy light regimes In our narrowed focus on the effects of oil in tropical environs, we will incorporate considerations specific to the habitat into what we Chapter | 27 Effects of Oil in the Environment 1011 already purport to know about general oil effects In this way, we not only are efficient; we also distinguish a few of the unique considerations we may face when oil spills in such places The elevated temperature regime likely to be encountered in tropical spills imposes a number of confounding factors on assessment of real and projected oil effects Warmer temperatures will accelerate the processes of weathering; thus, responders will need to be mindful of the dynamic setting in which they are examining toxicity Volatile fractions of the spilled oil will disappear rapidly, leaving behind a potentially very different toxicological mix Physical characteristics will change considerably from night to day and from shade to direct sun What is a liquid pool at noon may solidify in place by dusk Potential for vertical movement down into beaches and sediments may be a factor if the spilled products shift from one state to the other Under these conditions, all of our basic toxicological and effects rules and guidelines articulated above still apply Temperature, however, will be a primary determinant of exposure and chemical composition One physical characteristic of tropical environments that has the potential to substantially alter the spill toxicology of a given incident is the role of light in changing the chemistry and pathology of spilled products The interplay of ultraviolet (UV) radiation with the toxicity of oil components like PAHs has been known for many years Mottram, Doniach, and Doniach (in 1938 and 1939) documented light-mediated PAH toxicity with the single-celled organism, Paramecium caudatum.50,51 The clarity of water in many tropical regimes, combined with the intensity of sunlight (especially in summer months and closer to the equator), may result in conditions that can drastically alter the toxicity of oil to exposed organisms Specifically, intense sunlight may provide high enough energy to alter the chemical structure of compounds in the oil and serve to dramatically increase toxicity The mechanism for this toxicity has been summarized by Pelletier et al.52 Phototoxicity occurs when UV radiation is absorbed by the conjugated bonds of PAH molecules, exciting them to a higher energy state The absorbed energy is transferred from the excited PAHs to ground-state dissolved oxygen, forming singlet-oxygen intermediaries The resulting singlet oxygen and other oxygen free radicals are highly oxidizing and can destroy biomolecules in tissues The half-life of singlet oxygen is extremely short in seawater (~2 s) but is much greater in lipophilic tissues where hydrophobic PAHs accumulate, resulting in the greater potential for tissue destruction Ironically, several of the photoxicity studies we reference below involve light conditions not for the intense exposures expected in tropical waters, but in much more moderate conditions: midlatitude freshwater lakes, or subarctic marine waters For example, Landrum et al studied the apparent changes in toxicity of anthracene and benzo(a)pyrene in freshwater fish and water fleas.53 These authors determined that the observed increases in toxicity (sometimes hundreds 1012 PART | X Effects of Oil in the Environment of times greater than previously reported concentrations) resulted from photomodification of bioaccumulated PAHs rather than from photodegradation products Similarly, Barron and Ka’aihue noted that ultraviolet light increased the apparent toxicity of oil products, weathered oil, and PAHs as much as 2e1000 times.54 They also supported the mechanism of phototoxicity described above by Pelletier et al in which the mechanism of toxicity appeared to occur through a process of photosensitizationdin which the bioaccumulated chemical transfers light energy to other molecules causing toxicity through tissue damagedversus photomodificationdactual chemical transformation of a chemical by light energy According to Barron and Ka’aihue, the available evidence indicates that the phototoxic components of oil are individual three- to five-5 ring PAHs and heterocycles Determinants of photoenhanced toxicity include the extent of oil bioaccumulation in aquatic organisms and the spectra and intensity of UV exposure The potential hazard of photoenhanced toxicity may be greatest for embryo and larval stages of aquatic organisms that are relatively translucent to UV and inhabit the photic zone of the water column and intertidal areas What does this mean for oil spill response? It suggests that light-induced changes to oil-related compounds bioaccumulated into the transparent and translucent earlier life stages of marine organisms are more apt to be found in the upper photic zones of the water column and could amplify the anticipated effects of a spill We could conjure a very bad scenario in which a spill of oil occurred coincident with the mass spawning event of, say, corals Not only would a large toll be inflicted by the oil alone, but potentially significant additional impacts could be expected from photoenergized PAHs incorporated into the lipid-rich tissues of planktonic life stages One cautionary note about phototoxicity: McDonald and Chapman suggested that while processes and mechanisms of phototoxicity are well demonstrated and well described, their relevance to environmental management is less clear.55 They argue that phototoxic effects are in fact ameliorated by physical, chemical, and biotic factors (such as the presence of dissolved organic carbon, humic materials, or particulate matter; artificiality of laboratory exposure environments; physiological or behavioral adaptations of exposed organisms; and sensitive life-stage habitat preferences) The authors noted that at the time of their article, no studies existed that “clearly and directly implicate PAH phototoxicity with adverse ecological effects in field populations.” They quote Swartz et al.56 who state that the results of PAH phototoxicity studies to date ‘‘may be toxicologically correct, but ecologically irrelevant.’’ They recommended that management decisions not be based solely on a single line of evidence, such as phototoxic potential, until more compelling links to real-world impacts are made Chapter | 27 Effects of Oil in the Environment 1013 27.10 ARCTIC ENVIRONMENTS Arctic or Antarctic habitats are known (or have been known, until recently) for cold temperatures and unique physical features provided by ice and seasonally restricted or unrestricted access to light As was the case for tropical habitats, when we think about the impacts of oil in these environments, a logical approach is to consider how their unique characteristics might or might not alter the general statements about oil effects we have made to this point Rice et al included a discussion of the effect of temperature on apparent toxicity of oil mixtures.42 With their focus on Alaskan conditions, they obviously emphasized lower temperatures They identified two primary effects of low temperatures on the toxicity of aromatic hydrocarbons that were difficult to separate: increased toxicity due to increased persistence of aromatic hydrocarbons in water; and increased toxicity due to physiological modification of exposed organisms The flip side of the effects-of-temperature coin we discussed above might be expected for cold water environments: physical characteristics of spilled oil will be driven toward more viscous, perhaps solid states, and slower weathering The implications for oil effects assessment would include a potentially longer environmental residence in the absence of directed cleanup efforts and a more stable/consistent chemical composition for the spilled product Rice et al.’s comparison of similar fish and invertebrate species from cold and warmer waters suggested that cold-water organisms were more sensitive, but differences were not great and were attributed to temperature-driven considerations of oil persistence.42 However, a broader examination of the effect of water temperature on oil toxicity revealed an inconsistent and variable relationship between the two, and this finding suggests that temperature alone may not be a significant influence for differences in oil toxicology It is possible (and, it should be noted, speculative on our part) that unique physiological adaptations to life in cold-water environments (see Portner57and Abele and Puntarulo58) may represent risk factors for inhabitants of polar waters Some examples include the following: Sidell studied the physiology of high-lipid content in Antarctic fish.59 We might ask, how would the presence of lipophilic petroleum derivatives affect the function of this adaptation? Sidell and O’Brien discussed a unique feature of Antarctic icefishes (Family Channichthyidae): their lack of hemoglobin.60 How might oil interfere with the alternative physiological mechanism for transporting oxygen in these fish? The authors also noted that the constantly cold Antarctic waters are nearly completely oxygen-saturated Will this affect how oil behaves and the kinds of effects it will have on exposed organisms? We cannot answer these questions now, but perhaps with the renewed interest in oil leasing in arctic waters, opportunities will arise to pursue research questions of this type for indigenous resources 1014 PART | X Effects of Oil in the Environment A topic that likely has more relevance to spill remediation than assessment of spill effects is oil biodegradation, which is an important mechanism for reducing hydrocarbon levels in the environment It occurs as a natural process and as the key piece of a directed human cleanup strategy called bioremediation As the term suggests, biodegradation is driven by organismsdin this case, microorganisms such as bacteria and fungidthat utilize hydrocarbons as a food source and thereby break oil down into less complex and ultimately less toxic compounds While few biodegradation studies have specifically focused on high-latitude regions, related microbiological investigations have shown that temperature is a critical parameter for rates of degradation That is, biodegradation has been reported to occur more rapidly in warm temperatures (>10 C), suggesting that biodegradation and bioremediation would not be advisable in arctic or Antarctic spill situations However, Pelletier et al evaluated biodegradation in sub-Antarctic intertidal sediments and found that in fact low seawater temperatures (3e4 C) had no effect on oil-degrading communities and rates.61 This suggests that at least in some cases, low temperatures may not out-of-hand preclude the use of some traditional or typical approaches for reducing both exposure and toxicity, such as bioremediation 27.11 ECOLOGICAL EFFECTS OF OIL SPILLS Having labored through the process of trying to describe the narrowly focused effects of oildon organisms, on their physiology, and on cellular functionsdit should be apparent that the task of describing, in general terms, the broader ecosystem or ecological effects is many times more complex and difficult This, however, does not mean that summaries and syntheses have not been attempted, as the need has been recognized for decades Templeton reviewed a number of oil effects and oil spill studies current to that date, but did not synthesize the information into more general observations of effects at higher levels of biological organization, such as habitats.62 A conference held in 1978 (American Institute of Biological Sciences63) attempted to both, review and synthesize The proceedings brought together a wealth of information, but while the final day of the workshop was devoted to identifying future directions and research needs, the synthesis of the information was generally left to the reader Teal and Howarth reviewed seven oil spills that occurred after 1975 (the publication date of the benchmark National Academy of Sciences report on Petroleum in the Environment).64 They noted that: Oil spills have produced measurable effects on ecosystems that have not been readily predictable from laboratory studies on isolated organisms However, ecosystem-level interactions are poorly understood even without the complications resulting from effects of pollution Chapter | 27 Effects of Oil in the Environment 1015 Teal and Howarth defined eight questions on which to concentrate in their review:64 How long does spilled oil persist in marine systems? Does spilled oil sink, and by what mechanisms? What are the effects of oil on benthic and littoral systems? What are the effects of oil on plankton, and what is their importance? What are the effects on fish and fisheries? What are the effects of crude oil versus refined products? Can experimental studies be used to infer effects from actual spills? Can ecosystem effects be inferred from effects on individual species? They used the questions as a framework for deriving some general lessons from the seven spills.64 These yielded five empirical generalizations: Oil regularly reaches sediments after a spill Oil is persistent in anoxic sediment conditions Oil contaminates zooplankton and benthic invertebrates Fish are contaminated to a lesser extent Oil decreases abundance and diversity of benthic communities Clark et al reported on the effects of a chronic leak of a U.S Navy special fuel oil from an unmanned troopship that grounded on the rocky intertidal shoreline of northern Washington State.65 They documented continued exposure to the oil over a five-year period During the first year, dead and abnormal sea urchins and deformed seaweeds were observed near the wreck itself Despite the short-term shifts in intertidal communities, long-term community balance was not apparently affected Similarly, Coats et al monitored long-term impacts to the intertidal communities affected by the Exxon Valdez oil spill in Prince William Sound, AK.66 Although substantial inherent environmental variability presented challenges to the tracking of both effects and recovery, the authors determined that short-term impacts from both oil and cleanup (high-pressure hot water washing) faded after around three to four years The apparent recovery of intertidal communities was contrasted to longer-term impacts reported in other communities studied after the Exxon Valdez Harwell and Gentile reviewed over 300 papers related to the Exxon Valdez spill from both government and Exxon Mobil sources.67 They applied a risk assessment paradigm to evaluate a range of organisms from invertebrates to seabirds and marine mammals, and concluded that those resources not in decline at the time of the spill recovered within six years, with others approaching recovery by 15 years post-spill Notable exceptions were those ecosystem attributes related to orca pods This was a very different outcome from that found in a similar analysis by Peterson et al., who concluded that persistent low-level exposures to residual oil from the Exxon Valdez oil spill continued to cause impacts to wildlife 1016 PART | X Effects of Oil in the Environment through indirect effects and cascades within the ecosystem.68 It might be worth mentioning that the two sets of authors were funded by opposing interests in the debate over ongoing effects from this spill: Harwell and Gentile by ExxonMobil, and Peterson et al by the state and federal trustees Landis analyzed this very situation, asking why such stark differences existed between the results of the authors.69 He concluded that at least part of the difference could be explained by the infusion of different social values or policy goals into the science, what he termed “normative science.” This is beyond the purview of our discussion here, but the reader is referred to the original papers for further insights into this related but sidebar topic The interpretive difficulties imposed by natural environmental variability was acknowledged by researchers monitoring impact and recovery from other large oil spills Newey and Seed described rocky intertidal conditions following the Braer spill off the coast of Shetland (Scotland) in 1993 and spoke of the controversies that sometimes arose stemming from the problem of determining when naturally variable systems subject to a variety of stochastic events have returned to pre-spill states.70 Newey and Seed described the rocky intertidal as a mosaic of patches of biological communities in different successional stages depending on the timing of the event responsible for creating the patch They noted, as had previous spill researchers (e.g., Southward71,72), that oils spills imposed a relatively uniform pattern of development on the shore, with a reduced degree of community diversity They estimated that recovery on such shorelines could take as long as 10 or more years Jackson et al were researchers working at the Smithsonian Tropical Research Institute in Panama, when more than million liters of medium weight crude oil spilled from a storage tank on the Caribbean coast.73 It was the largest spill into sheltered coastal habitat in the tropical Americas As such, these researchers were uniquely positioned and qualified to document the shortand long-term effects of the release across a range of coastal tropical resources, including mangroves, sea grasses, intertidal reef flats, and subtidal reefs Importantly, the large group of authors interpreted their observations within areas of specialization, and in a larger context of patterns and significance They noted where documentation of damage matched that for previous spills assessments, as in a higher degree of disruption and disturbance to sheltered communities vis-a`-vis those along open coasts However, they also noted areas where their results diverged from those of other oil impact studies, as in the record of extensive mortalities of subtidal corals and sea grass infauna Jackson et al also recorded a range of sublethal impacts and inferred longer-term effects to the tropical system communities than was evident from initial mortalities.73 The latter assertionsdthat sublethal effects to key components of a given ecosystemdwould be echoed by researchers of another large spill, the Exxon Valdez spill in Prince William Sound We have already discussed the actual and projected long-term impacts of that event to orca whales (Matkin et al.30) and to pink salmon (Heintz et al.19) Heintz addressed this question directly, by Chapter | 27 Effects of Oil in the Environment 1017 modeling a pink salmon population over a 70-year period and overlaying PAH effects determined from previous studies and randomly varying density dependence on the simulated salmon run.74 Heintz determined that conditions of 100% exposure to a hypothetical spill resulting in an aqueous PAH concentration of 18 nL/L (nanoliters per liter) would cause an 80% decrease in population productivity and 11 percent probability of extinction after 35 generations (i.e., 70 years) The overall population growth rate, however, declined by only 5% The modeling showed that for low-exposure levels, density dependence compensated for reduced population size and appeared to buffer or mediate against population extinction However, if the equilibrium size is sufficiently reduced, the buffering capacity is overwhelmed by random environmental variation and the risk of extinction increases The Exxon Valdez Oil Spill Trustee Council has tracked trends in recovery of many individual impacted resources and has worked to interpret the results in the context of the overall health of Prince William Sound as an integrated whole The reader is referred to the many publications and references generated from this ambitious and long-term effort.75 In marsh habitatsda critical environment that we have not discussed in any detail to this pointdeffects studies have shown that oil spills can have long-term impacts Marshes are frequently defined by limited water circulation and exposure conditions, which contribute to persistence of spilled oil Culbertson et al reported on continued adverse impacts to Spartina marsh grass 37 years after a barge spill of No fuel oil in Buzzards Bay (MA), which resulted in sediment instability, topographic changes, and habitat loss.76 The 1974 Metula supertanker spill in the Strait of Magellan, Chile, provided a stark contrast for large oil spills occurring in high latitudes because there was virtually no cleanup of the spilled light Arabian crude oil Particularly impacted shorelines included sheltered gravel beaches and marshes Follow-up visits to assess the extent of recovery (e.g., Owens et al.; Shigenaka et al.; Gundlach; Baker et al.77-80) revealed a slow pace of recovery, particularly in the marsh This spill, in a remote portion of Patagonia, represented one end of the spectrum of oil spill impact and confirmed that, unabated, large quantities of oil released into the environment result in substantial, profound, and long-term consequences The common conclusions drawn from larger perspective analyses of oil effects in very different spill settings may be that less apparent, sublethal effects have the potential to significantly affect the fundamental structure of regional ecosystems and the long-term viability of key members of those systems; and that overwhelming amounts of oil released into the environment result in visible, measurable, long-term impacts 27.12 THE FUTURE OF OIL EFFECTS SCIENCE It should be apparent that we have learned a great deal about oil effects It should also be apparent that there remains much that we not know 1018 PART | X Effects of Oil in the Environment Throughout this chapter, we have identified specific knowledge gaps, which might be used as the basis for ongoing research Almost from the beginning, we have consistently focused on aromatic hydrocarbons as the petroleum constituents of concern in considering the toxicity of oil We not know the significance, if any, of most of the many other chemical constituents of oil Even for PAHs, we not understand very much about mechanisms of toxicity Our abilities to model oil spill impacts are rudimentary, largely because of the lack of information.81 Application of what we know about effectsdthe surprising impact of very low concentrations of weathered oil, for exampledremains unclear That is, how we manage environmental exposures at the limits of what we are able to reliably measure and comprehend? New techniques offer some promise in being able to provide a more detailed but holistic picture of oil effects to individual organisms Examples include molecular diagnostic technologies (e.g., Downs et al.) that can trace back to physiological impairment to specific enzyme functions and cellular processes.82 This technique has been used to evaluate exposure and mechanisms after the Exxon Valdez oil spill, but further refinement and validation would greatly improve its utility as a tool for understanding the past and current effects of oil in an environment of interest Anderson and Lee reviewed numerous molecular, cellular, and physiological biomarkers and concluded that there were differences in organism responses to two- and three-ring PAHs (associated with petroleum) versus four- and five-ring PAHs (associated with combustion).83 When mixtures of PAHs exist at spill locations, interpretation of biomarker results can be rendered difficult They concluded that at the present time, the links between biomarkers and higher order biological endpoints (e.g., toxicity, reproductive failure) was not well established This represents an area of potentially high return for research activities As we discussed in the preceding section, specific issues related to oil spill effects in high-latitude regions are not well articulated and have not been revisited in North America (it should be noted that Norwegian researchers have focused on at least some of these, for reasons that should be apparent) since the initial push to develop offshore continental shelf regions of Alaska in the 1970s Warming of arctic waters in particular has spurred much renewed interest in new leases and thus represents both risk (of spills in challenging conditions) and opportunity (to better determine what the risks are) After some promising attempts to institutionalize and fund oil spill research in the United States, it appears that we have reverted to external drivers (e.g., leasing and large spills) as determinants of research support availability We can be hopeful, but the current global economic climate suggests that there will be significant competition for research dollars (euros, yuan, rupees) well into the foreseeable future Chapter | 27 Effects of Oil in the Environment 1019 27.13 SUMMARY AND CONCLUSIONS We began this conversation by referring to the empirical science and the predictive art involved in toxicology and estimation of oil effects We have endeavored to guide the reader through a number of different conceptual frameworks for interpreting what we know and how we apply it to the specifics of a given spill incident to define risk The 2003 update of Oil in the Sea (National Research Council, 2003) noted the progress made toward understanding the toxic effects of petroleum in a variety of organisms and environments We continue to make progress, particularly with respect to better defining mechanisms of how oil can be harmful at the organism, physiological, and cellular levels We also have a better idea of how those impacts translate and extrapolate to population and community levels, and we have identified examples in real spills that appear to show this However, the needs articulated in 2003 (e.g., understanding of natural variability, assessment of higher level effects of spill events, influence of longterm climatic and global-scale shifts on impact and recovery assessments, etc.) remain, and other questions stemming from new scientific insights have arisen The recent determination of how specific aromatic hydrocarbons exert their toxicity on fish is a promising development toward the goal of forecasting the effects of hydrocarbon mixtures on organisms of concern The ability to understand the long-term consequences of sublethal exposures is the basis for projecting future effects on populations and ecosystems Although the known reserves of petroleum are declining and production activities have peaked, oil will continue to be a significant part of the world’s energy portfolio for years to come As a result, we will continue to move oil; 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Aquat Tox 1999;253 82 Downs CA, Shigenaka G, Fauth JE, Robinson CE, Huang A Cellular Physiological Assessment of Bivalves After Chronic Exposure to Spilled Exxon Valdez Crude Oil Using a Novel Molecular Diagnostic Biotechnology Environ Sci Techn 2002;2987 83 Anderson JW, Lee RF Use of Biomarkers in Oil Spill Risk Assessment in the Marine Environment Hum Ecol Risk Assess 2006;1192 ... substantially from the fresh oil initially released It Chapter | 27 Effects of Oil in the Environment l l 991 is essentially a different kind of oil spill, even with a single original source oil These differences... rewind the tape somewhat to take another look at the physical chemistry of oil in water Chapter | 27 Effects of Oil in the Environment 1003 27. 7 OIL CHEMISTRY, PHYSICAL BEHAVIOR, AND OIL EFFECTS. .. to oil spills, in the wake of the Exxon Valdez This 1989 oil spill in Prince William Sound, Alaska (which remains the largest U.S spill in history) provided the impetus for more oil spill effects