Reports

The acute and chronic effects of wastes associated with offshoreoil and gas production on temperate and tropical marine

ecological processes

Douglas A. Holdway*

Department of Biotechnology and Environmental Biology, Royal Melbourne Institute of Technology University, Bundoora West Campus,

GPO Box 71, Bundoora, Melbourne, Vic. 3083, Australia

Abstract

A review of the acute and chronic effects of produced formation water (PFW), drilling fluids (muds) including oil-based cutting

muds, water-based cutting muds, ester-based cutting muds and chemical additives, and crude oils associated with offshore oil and

gas production was undertaken in relation to both temperate and tropical marine ecological processes. The main environmental

effects are summarized, often in tabular form. Generally, the temporal and spatial scales of these studies, along with the large levels

of inherent variation in natural environments, have precluded our ability to predict the potential long-term environmental impacts

of the offshore oil and gas production industry. A series of critical questions regarding the environmental effects of the offshore oil

and gas production industry that still remain unanswered are provided for future consideration. � 2002 Elsevier Science Ltd. Allrights reserved.

Keywords: Produced formation water; Drilling fluids; Crude oils; Acute toxicity; Chronic toxicity; Future research priorities

1. Introduction

There are a variety of wastes produced by or associ-ated with offshore oil and gas production. These includeproduced formation water (PFW), drilling fluid chemi-cals, oil-based drilling muds and cuttings, water-baseddrilling muds and cuttings, and of course oils includingboth crude oil from extraction processes and fuel/dieseloil from ships and equipment used in the production ofoil and gas. This review will look at the associated acuteand chronic toxicity of the above wastes on tropicaland temperate marine organisms from a wide varietyof ecosystems including plankton communities, benthiccommunities, pelagic communities, sea grass beds,mangroves and coral reefs.

2. Produced formation water

Produced formation water, the oily water usuallydischarged from a platform after separation from the

oil, is made up from formation water (water associatedwith the oil in the reservoir) and potentially includeswater which was injected into the reservoir to maintainpressure and oil production. The volumes of PFWproduced are enormous it is estimated that 234 milliontonnes of PFW were discharged into the UK sector ofthe North Sea alone in 1997 (Henderson et al., 1999). Itis estimated that 7500–11,500 tonnes of petroleum hy-drocarbons enter the environment each year from PFWdischarges globally (Black et al., 1994a,b). As oil fieldsage, the volume of PFW can increase to several times thevolume of oil produced (Henderson et al., 1999).The hydrocarbon content of formation water, which

generally makes up the bulk of produced water, is only asmall part of the total organic composition and is gen-erally restricted to a maximum oil content of 40 mg/l orless (Brendehaug et al., 1992). Most of the hydrocarbonmaterial is made up of naturally produced low molec-ular weight organic compounds along with a variableamount of chemicals used in the production process(Davies and Kingston, 1992). These hydrocarbons in-clude residual volatile compounds, as well as non-vola-tile hydrocarbons not removed by the separation regimeutilized on the platform. Environmental effects of PFWs

www.elsevier.com/locate/marpolbul

Marine Pollution Bulletin 44 (2002) 185–203

*Tel.: +61-3-9925-7107; fax: +61-3-9925-7110.

E-mail address: d.holdway@rmit.edu.au (D.A. Holdway).

0025-326X/02/$ - see front matter � 2002 Elsevier Science Ltd. All rights reserved.PII: S0025-326X(01 )00197-7

are thus related to their specific chemical compositions,which vary greatly between platforms. There are a va-riety of fates that the discharged materials can havewithin the marine environment including volatilizationto the atmosphere, adsorption and settling out onto thebottom sediments, dispersal by water currents, and up-take and metabolism by both pelagic and benthic ma-rine organisms.

2.1. Acute toxicity of produced formation waters

Given the variety of chemicals and range of concen-trations possible, it is difficult to generalize about thepotential toxicity of any particular PFW other than bydescribing the toxicity of the various individual com-ponents and then attempting to predict the mixture-toxicity based on the single toxicant toxicity’s. Since thisapproach is very susceptible to error, the best way ofassessing potential environmental impact is to assess‘‘whole PFW’’ toxicity using a variety of living organ-isms, preferably indigenous marine ones. This has beenthe approach adopted by most regions of the world andacute toxicity data from various production areas indi-cated a relatively low acute toxicity to various marineorganisms with acute LC/EC50’s ranging from roughly5% to 50% whole PFW (Table 1).

In addition to the complex mixture of aliphatic, aro-matic and polar compounds in PFW which contribute tothe relatively modest acute toxicity of produced water,there are a number of production chemicals which areadded for different purposes through the process orseparation line including corrosion inhibitors, scale in-hibitors, demulsifiers, flocculents, anti-foaming agentsand biocides (Brendehaug et al., 1992). The acute tox-icity of such chemicals contributes to the overall toxicityof PFW water and the differences in toxicity betweensuch chemicals can be up to 4 orders of magnitude(Table 2). Thus, the varying concentrations of suchchemicals in different PFWs along with the large differ-ences in their acute toxicity explains the reported 10-folddifference in toxicity between different PFWs dependingon the level of such chemicals in each (Black et al., 1994a;Brendehaug et al., 1992; Burns et al., 1999; Davies andKingston, 1992; Henderson et al., 1999; Holdway andHeggie, 1998; Neff et al., 1992; Rabalais et al., 1992;Terrens and Tait, 1994, 1997; Tollefsen et al., 1998).It is interesting that water-soluble production chem-

icals do not always increase the toxicity of the aqueousphase of PFWs compared to oil soluble productionchemicals, though there is evidence that some produc-tion chemicals may increase the solubility of oil com-ponents of PFWs (Henderson et al., 1999). Overall,however, the acute toxicity of PFWs to marine organ-

Table 1

Acute toxicity of various produced formation waters (PFWs)

Organism tested PFW Test conditions EC/LC50 (% PFW) Reference

Microtox (Vibrio fischeri) Bass Strait Platforms

(average of 10 platforms)

15 min static 7.09 Black et al. (1994b)

Brine shrimp (Artemia salina) Bass Strait Platforms

(average of 10 platforms)

24 h static 58.8 Black et al. (1994b)

Marine amphipod

(Allorchestes compressa)

Halibut Platform, Bass

Strait

96 h static replacement 34.5 Terrens and Tait (1994)

Mysid shrimp

(Mysidopsis bahia)

Western Outer Continental

Shelf, Gulf of Mexico

96 h daily renewal 7.08 (n ¼ 24,S.D.¼ 3.73); 10.05(n � 400,S.D.¼ 10.36)

Moffitt et al. (1992)

Mysid shrimp

(Mysidopsis bahia)

Western Outer Continental

Shelf, Gulf of Mexico

7 days daily renewal 5.77 (n ¼ 24,S.D.¼ 2.48)

Moffitt et al. (1992)

Mysid shrimp

(Mysidopsis bahia)

Krisna and Widuri

Platforms, West Java Sea,

Indonesia

96 h daily renewal

using 96 h biodegraded

produced water

25 (n ¼ 3) –Krisna; 55 (n ¼ 3) –Widuri

Smith et al. (1998)

Silverside fish

(Menidia beryllina)

Krisna and Widuri

Platforms, West Java Sea,

Indonesia

96 h daily renewal

using 96 h biodegraded

produced water

45 (n ¼ 3) –Krisna; 25 (n ¼ 3) –Widuri

Smith et al. (1998)

Sheepshead minnow

(Cyprinodon variegatus)

Western Outer Continental

Shelf, Gulf of Mexico

96 h daily renewal 21.55 (n ¼ 23,S.D.¼ 6.99); 19.21(n � 400,S.D.¼ 14.82)

Moffitt et al. (1992)

Sheepshead minnow

(Cyprinodon variegatus)

Western Outer Continental

Shelf, Gulf of Mexico

7 days daily renewal 19.72 (n ¼ 23,S.D.¼ 7.71)

Moffitt et al. (1992)

Algae (Skeletonema costatum) Gullfaks, North Sea 24 h growth inhibition 27.6 (n ¼ 8) Brendehaug et al. (1992)

Algae (Skeletonema costatum) Statfjord, North Sea 24 h growth inhibition 34.8 (n ¼ 5) Brendehaug et al. (1992)

Microtox (Vibrio fischeri) Gullfaks, North Sea 15 min static 7.18 (n ¼ 8) Brendehaug et al. (1992)

Microtox (Vibrio fischeri) Statfjord, North Sea 15 min static 4.66 (n ¼ 5) Brendehaug et al. (1992)

186 D.A. Holdway / Marine Pollution Bulletin 44 (2002) 185–203

isms is low and would likely only have acute effectswithin the immediate mixing zone around a productionplatform.Acute effects of PFWs reported to occur in the mix-

ing zone include: altered benthic communities domi-nated by short-lived opportunistic polychaetes up to100 m from offshore platforms (Neff et al., 1992); de-creased abundance of barnacles on platform structures;and mortality of oysters within 23 m of an outfall(Black et al., 1994a,b). Most distribution models predictthat acute toxicity due to exposure to PFW will benegligible outside the mixing zone (Brendehaug et al.,1992). In a study of produced waters from two plat-forms located in the West Java Sea, Indonesia, Smithet al. (1998) found that acute toxicity was only likely tooccur at low levels not exceeding 5% based on predictedbody residues and a time-varying integrated physico-chemical transport model. Use of such models to esti-mate the risk of acute toxicity is a useful method topredict toxicity in areas exposed to plumes in which theactual exposure concentrations will vary with time andspace. However, it must be remembered that models aredefined as ‘‘non-working copies of the original’’ andthat they are only as good as the quality of the dataused to create them.

2.2. Chronic toxicity of produced formation waters

There are far less data available regarding the chroniceffects of PFWs. Some of the potential effects includeimpacts on the surface microlayer surrounding hydro-carbon production platforms, altered benthic communityspecies composition, altered behavior and physiology,reduced growth, and decreased fecundity of laboratoryexposed organisms using short-term chronic toxicity tests(Black et al., 1994b; Brendehaug et al., 1992; Din andAbu, 1992; Hinkle-Conn et al., 1998; Krause, 1995;Krause et al., 1992; Moffitt et al., 1992; Neff et al., 1992;Osenberg et al., 1992; Rabalais et al., 1992; Raimondiand Schmitt, 1992; Reed et al., 1994).

Chronic effects have been reported in filter-feedingorganisms exposed to crude oil terminal PFW concen-trations as low as 0.08 ppm while other studies havefound no effects at PFW concentrations ranging from1.6% to 11.7% (Table 3). Sublethal effects such as alteredliver enzyme activities in reef fish living in close vicinityto oil producing platforms indicate chronic exposure tolow levels of hydrocarbons but, as with most biomarkersof exposure, such effects are difficult to interpret relativeto potential deleterious population effects (Holdwayet al., 1995).In marine systems, many planktonic larval organisms

and early developmental stages could potentially beexposed to plumes of PFWs and there is some evidencethat exposure of early life stages to low concentrationsof PFWs can cause a developmental response at a laterstage in sea urchins (Krause et al., 1992). Given thatplanktonic larvae must generally undergo a sensitivetransition phase during which they settle and undergometamorphosis into adult forms, exposure to toxicantscontained in PFWs during this important life historyevent could have pronounced effects.Exposure of laboratory-reared red abalone (Haliotis

rufescens) larvae which were transplanted into cages atvarying distances from a PFW diffuser near Carpinteria,CA, USA, resulted in significant effects on mortality,settlement, metamorphosis, viability, and swimmingbehavior at distances up to 500 m from the diffuser andconcentrations as low as 0.01% (100 ppm) PFW (Rai-mondi and Schmitt, 1992). The authors demonstratedfor the first time that planktonic larvae can be adverselyaffected by PFW plumes discharging into high energy,open coast environments and that the prevailing as-sumptions regarding lack of risk of PFWs to planktonicspecies in open coast environments were incorrect. Theyconcluded that there was a need for more complete as-sessments of both the ecotoxicological risk to mero-plankton and the population consequences of PFWdischarges.In a second study of the same PFW source, giant kelp

(Macrocystis pyrifera) recruitment was found to be

Table 2

Acute toxicity of chemicals added in the process/separation line

Chemical type Acute toxicity EC50 (mg/l)

Algae

(Skeletonema costatum)

Brine shrimp

(Artemia salina)

Microtox (Vibrio fischeri)

(minutes exposed)

Reference

Corrosion inhibitor 0.2–2 >20–25 15–50 (15); 7.1–21.9 (5–30) Brendehaug et al. (1992),

Henderson et al. (1999)

Scale inhibitor 60 1000 >1000 (15) Brendehaug et al. (1992)

Demulsifier 20 30 20 (15); 2.1–112 (5–15) Brendehaug et al. (1992),

Henderson et al. (1999)

Flocculent >1000 >15,000 >15,000 (15) Brendehaug et al. (1992)

Anti-foam 120 150 9 (15); 5.4 (5) Brendehaug et al. (1992),

Henderson et al. (1999)

Biocide – – l5.2–33.7 (15–45) Henderson et al. (1999)

D.A. Holdway / Marine Pollution Bulletin 44 (2002) 185–203 187

affected only in regions very close to the outfall (<50 m)and that the lack of sporophyte production was proba-bly due to factors affecting gametophyte survival (Reedet al., 1994). Although concentrations of 10% PFWwere required to show field effects, laboratory exposuresto PFW concentrations as low as 0.01% caused a 2-foldreduction in the proportion of females extruding eggs andproducing sporophytes. Exposure to 1% PFW in thelaboratory also affected the chemical recognition betweenmale and female gametes and caused a reduction in theamount of sperm available for fertilization (Reed et al.,1994). Thus, the authors are unable to conclude thatM.pyrifera are less sensitive to PFW since lower apparentfield effects were contrasted with higher laboratory sen-sitivity than other organisms previously studied.

A third study of marine organisms exposed to PFWfrom a diffuser near Carpinteria, CA,USA, looked at twospecies of mussels (Mytilus californianus and Mytilusedulis) transplanted to the field. This study found dis-tance-from-source-dependent sublethal effects occurredin both species of mussels exposed to PFW as measuredby shell growth and condition (Osenberg et al., 1992).The difficulties in interpreting spatial effects in marineinvertebrates were discussed and it was noted that ma-rine organisms with a planktonic dispersal stage tend todecouple local production of propagules from subse-quent recruitment into the local adult population.Osenberg et al. (1992) also found differences in benthicinfaunal distributions with distance from the PFW dif-fuser, with nematodes being more abundant closer to

Table 3

Chronic toxicity of various produced formation waters (PFWs)

Organism tested PFW Test conditions Endpoint (units of PFW) Reference

Asian clam

(Donax faba)

Bintulu crude oil terminal

(COT), Bintulu, Sarawak,

Malaysia

12 days of static

exposure in 150 l tank

Clearance rate:

LOEC¼ 8.6 ppm (n ¼ 4)Din and Abu (1992)

Respiration rate:

LOEC¼ 8.6 ppm (n ¼ 4)Scope for growth:

LOEC¼ 8.6 ppm (n ¼ 4)

96 h of static

exposure in 15 l

LC10¼ 8.6 ppmLC20¼ 11.1 ppmLC40¼ 14.7 ppm

Asian clam

(Donax faba)

Lutong COT, Miri,

Sarawak, Malaysia

12 days of static

exposure in 150 l tank

Clearance rate:

LOEC¼ 0.75 ppm (n ¼ 4)Din and Abu (1992)

Respiration rate:

LOEC¼ 0.75 ppm (n ¼ 4)Scope for growth:

LOEC¼ 0.75 ppm (n ¼ 4)

96 h static exposure

in 15 l

LC10¼ 0.75 ppmLC20¼ 1.10 ppmLC40¼ 1.65 ppm

Asian clam

(Donax faba)

Labuan COT, Labuan,

Malaysia

12 days of static

exposure in 150 l tank

Clearance rate:

LOEC¼ 0.08 ppm (n ¼ 4)Din and Abu (1992)

Respiration rate:

LOEC¼ 0.08 ppm (n ¼ 4)Scope for growth:

LOEC¼ 0.08 ppm (n ¼ 4)

96th static exposure

in 15 l

LC10¼ 0.08 ppmLC20¼ 0.11 ppmLC40¼ 0.14 ppm

Mysid shrimp

(Mysidopsis bahia)

Western Outer Continental

Shelf, Gulf of Mexico

7 days of daily

renewal

Survival: NOEC¼ 3.14%(n ¼ 24, S.D.¼ 1.92)

Moffitt et al. (1992)

Growth: NOEC¼ 1.60%(n ¼ 24, S.D.¼ 1.41)Fecundity: NOEC¼ 2.20%(n ¼ 24, S.D.¼ 1.38)

Sheepshead minnow

(Cyprinodon variegatus)

Western Outer Continental

Shelf, Gulf of Mexico

7 days of daily

renewal

Survival: NOEC¼ 11.7%(n ¼ 23, S.D.¼ 6.66)

Moffitt et al. (1992)

Growth: NOEC¼ 2.75%(n ¼ 23, S.D.¼ 2.17)

188 D.A. Holdway / Marine Pollution Bulletin 44 (2002) 185–203

the diffuser, but reduced abundance of most carnivorousgroups including nemerteans, and several families ofpolychaetes.In a study of sea urchin fertilization success using the

same PFW from Carpinteria, Krause et al. (1992)showed that even at the lowest PFW concentrationtested (0.0001% or 1 ppm), fertilization success wassignificantly reduced by as much as 10–20% from con-trols though a substantial fraction (>50%) were suc-cessfully fertilized at the highest concentration tested of1%. Such effects were later shown to exhibit significanttemporal variability though spatial variability was lowand the general spatial pattern of toxicity along atransect was relatively constant (Krause, 1995). Use ofan embryo developmental test in the laboratory showedthat effects arising from sperm exposure were far greaterthan those arising from egg exposure to PFW (Krauseet al., 1992). This was as a result of delayed expressionof effects of sperm exposure until later on in the em-bryonic development. The authors suggest that thetoxicological mechanism most likely involves microtu-bule function in sperm, which could cause early retar-dation of development by delaying nuclear fusionthrough impaired centriole function. Other studies po-tentially also involving microtubule-mediated effectsinclude swimming and chemoreception of abalone lar-vae (Raimondi and Schmitt, 1992), swimming of kelpspores (Reed et al., 1994) and growth of mussels(Osenberg et al., 1992). The possibility that all of thesePFW effects could be mediated through a unifying tox-icological mechanism as suggested by Krause et al.(1992) is an important area for future research to predictPFW impacts in marine environments.Benthic community effects have been noted in areas

of coastal Louisiana, Gulf of Mexico, USA, receivingPFW discharges up to 800 m from the point of release(Rabalais et al., 1992). These effects were found for bothspecies numbers and individual species abundance’sthough impact distances varied greatly and ranged fromno effects to 800 m. Bioaccumulation studies usingoysters (Crassostrea virginica) showed that PFW con-taminants were taken up and accumulated by oystersboth in close proximity to discharges and also at dis-tances up to 1000 m from discharges. Contaminantsincluded polycyclic aromatic hydrocarbons (PAHs),trace metals and total radium which have been shown inother studies to be found in PFWs from the Gulf ofMexico region (Neff et al., 1992).In another study of PFW contaminated sediment,

juvenile spot (Leiostomus xanthurus) did not activelyavoid sediment contaminated with 22 mg PAH/kg drysediment (Hinkle-Conn et al., 1998). In fact, feedingstrikes increased dramatically in the high-density meio-fauna treatment with a 239% increase compared tocontrols, possibly as a result of burrowing avoidance bythe prey organisms (majority were harpacticoids in this

experiment). It was concluded that due to lack ofavoidance or reduction in feeding intensity by spot,there was an increased likelihood that the fish wouldthus experience detrimental biological effects as a con-sequence of increase ingestion and exposure to the PAHcontaminants.Such effects can include elevated hepatic P-450E, aryl

hydrocarbon hydroxylase (AHH) activity, superoxidedismutase (SOD) activity, and ethoxyresorufin O-deethylase (EROD) activity, all substrate inducible en-zymes involved in PAH metabolism (Hinkle-Conn et al.,1998). Gill hyperplasia, pancreatic necrosis, reducedphagocytic activity of macrophages has also been re-ported in spot collected from PAH-contaminated sites.The authors conclude that continued feeding in areaswith sediment PAH contamination at or about 22 ppmwill likely lead to chronic exposure to PAH which couldcause increased susceptibility to disease from suppressedimmune function, reduced growth, and delayed sexualmaturity in fish.

3. Drilling fluids and chemicals

The drilling of wells also generate significant quanti-ties of wastes which have been estimated to account forup to 2% of the total waste volume generated in theUnited States (Reis, 1992). This waste is made up ofdrilling fluids and the cuttings generated during drilling.Drilling fluids (drilling muds) are used to remove cut-tings from the hole, prevent blowouts by controllingback pressure, maintain the integrity of the hole topermit the installation of a casing, and to cool andlubricate the drill bit.Other functions ascribed to drilling fluids include:

• supplying hydraulic power to the drill bit,• seal permeable formations of the borehole,• suspend cuttings when circulation is interrupted suchas when adding a new piece of drillpipe,

• support part of the weight of the drillstring throughbuoyancy, and

• ensure the securing of important information aboutthe formation being drilled to permit its successfulevaluation (Hinwood et al., 1994).

There are three major types of drilling fluids: water-based where the fluid phase is water, oil-based where thefluid phase is oil, and synthetic-based where the fluidphase is a synthetic base compound such as an ester(Burke and Veil, 1995). Water-based drilling fluids arethe most common and often contain a variety ofchemicals, which are formulated as required from agenerally limited list of additives. More than 90% of thetotal ingredients of most water-based drilling fluids usedoffshore in US waters consist of four materials: barite,

D.A. Holdway / Marine Pollution Bulletin 44 (2002) 185–203 189

bentonite, lignite and lignosulphonate (Hinwood et al.,1994). While more than 1000 products are available forformulating drilling fluids, the total number of ingredi-ents in most drilling fluids is in the range of 8–12.For example, the seven types of drilling muds that

make up some 89% of Italian offshore activities con-tained only nine significant products that were listed byTerzaghi et al. (1998) as follows:

• Lignosulphonate, a by-product of the separation ofpulp from wood using the sulphite process whichwhen added with iron and chrome is used as a disper-sant in water-based drilling fluids.

• Modified starch made from bacterially stabilized po-tato starch used to provide filtration control withlow viscosity.

• Soltex, an asphalt produced as a residue in petroleumrefining and sulphonated to make water-soluble, thatis primarily used for shale control.

• XC-polymer, a high molecular weight polysaccharideutilized as a viscosifier in fresh and salt water fluids.

• Mor-rex, a chemically modified enzyme-hydrolyzedcornstarch utilized as an effective dispersant in lime-treated muds.

• Carboxymethylcellulose (CMC) LV, a cellulose deriv-ative used as a fluid loss reducer and a shale inhibitor.

• Polyanionic cellulose (PAC) LV, another polymerused as a fluid loss reducer and shale inhibitor butwith greater tolerance towards salts.

• Wetting agent/detergent, a specially formulated blendof surfactants (including barite, calcite and haema-tite) used in water-based drilling fluids to minimizebit balling and to improve bit cleaning.

• Defoamer, a high molecular weight alcohol blendedwith fatty acid derivatives utilized as defoamingagent.

Government regulatory regimes for drilling fluidstraditionally used their chemical category to regulate thevarious classes of drilling fluids. Concerns were raised inthe 1980s regarding the effects of drilling fluids on theoffshore marine environment in the USA (Morse et al.,1986), resulting in tighter government regulations.Testing of drilling fluids and new additives is now arequired practice in the United States, Canada andEurope, and standards between countries can differ de-pending on their specific concerns and perspectives(Jones and Leuterman, 1990). Testing can also vary be-tween regions within a country and the cost of ensuringcompliance with such tests can limit the marketability ofthe various drilling fluid products.Recently, some governments have adopted alternate

approaches such as case-by-case assessment based onenvironmental impact assessment. Such approaches re-quire knowledge of specific location environmentalsensitivity, the amount of drilling fluid to be used and its

type, the potential for accumulation of cuttings, and theenvironmental characteristics of the drilling fluids to beused. Newer economic environmental management ap-proaches for drilling operations can result in up to 50%reductions in drilling waste management costs as well asminimization of environmental impacts (Longwell andAkers, 1992). The use of synthetic-based muds (SBMs),which involve the use of a synthetic liquid as the contin-uous phase of the mud while brine serves as the dispersedphase has been encouraged by various government en-vironmental requirements for drilling muds. The syn-thetic base compounds for such muds can be esterssynthesized from fatty acids and alcohols, polyalpha-olefins, or olefin isomers, all relatively non-toxic com-pounds (Burke and Veil, 1995).

3.1. Acute toxicity of drilling fluids

There is paucity of data on acute toxicity of drillingfluids of any kind, likely because of their relatively lowacute toxicity. Older oil-based drilling muds (OBMs)containing Number 2 diesel has greater toxicity than thelower-toxicity mineral and animal oils developed as basefluids. Such oil-based drilling muds are used in high-temperature formations; formations containing water-sensitive minerals, clays or reactive gases; and in wellswhere a high level of lubrication is needed (Reis, 1992).Use of oil-based muds today generally requires a reuse/recycling system since their cost is higher and manyareas of the world forbid their discharge (e.g., Gulf ofMexico). Other areas distinguish between diesel-basedmuds and mineral oil-based muds (e.g., North Sea),permitting the discharge of less toxic mineral oil-basedmuds on an individually approved basis (Bleier et al.,1993).Recently, fish oil esters have been successfully used as

replacements for mineral oils in oil-based drilling fluidsand they have been found to have even lower acutetoxicity to marine organisms, with LC50s for the algaeIsochrysis sp. and the post larvae prawn (Panaeusmonodon) greater than 100,000 ppm (10%) for bothBiogreen whole fluid and the BG5500 base fluid (Pappand West, 1999). Acute effects on the copepod Gladio-ferens imparipes were almost as non-toxic with a 48 hLC50 for the Biogreen whole fluid >100,000 ppm and the48 h LC50 for the BG5500 base fluid determined to be67,100 ppm or 6.71% (Papp and West, 1999).Synthetic-based muds are water in oil emulsions

proposed to replace OBMs owing to their technical andenvironmental advantages over OBMs and WBMs(Burke and Veil, 1995). A study to evaluate SBMcharacteristics found that they had low to moderateacute toxicity to brine shrimp (Artemia salina) and towater fleas (Daphnia magna) when tested in the labora-tory (Xiao and Piatti, 1995). These tests were not suffi-cient to ensure compliance with current legislation and

190 D.A. Holdway / Marine Pollution Bulletin 44 (2002) 185–203

approval of their use was uncertain at the time of pub-lication.The variety of chemical components in drilling muds

and their variation in both percentage composition andinherent acute toxicity means that there is the potentialfor large variations in toxicity between different muds.Using the major Italian drilling fluid components to il-lustrate this, it can quickly be seen that any drilling mudcontaining larger amounts of defoamer and wettingagents (both blends of surfactants) would have signifi-cantly higher toxicity (Table 4).The much higher toxicity of such compounds makes

their discharge into the sea ‘‘very concerning’’ accordingto the authors of this study (Terzaghi et al., 1998). Theauthors, however, recognize that it is important to assessany long-term effects of drilling muds and that simula-tion of actual drilling fluid dispersion is necessary tounderstand actual exposure concentrations and areas,and the dilution effects of the sea. According to Bleieret al. (1993), such ‘‘specialty additives’’ are now beingdeveloped to minimize toxicity problems and thatmodern drilling fluids use lower toxicity solutions toproblems that require such additives to ensure that theyare far less toxic than older formulations.

3.2. Chronic toxicity of drilling fluids

There is even less information regarding the chronicor long-term toxicity of drilling fluids to marine organ-isms. Some studies have addressed this aspect of bio-logical impact from a biodegradation perspective andlooked at the percentage ultimate biodegradation usingclosed-bottle anaerobic biodegradation testing. It hasbeen estimated that oil discharged on drilling cuttingswas the greatest source of oil pollution in the North Seafrom drilling operations, having peaked in 1985 at25,880 tonnes (Kingston, 1992). The response of benthicorganisms has been either a reduced number of indi-viduals with few species close to drilling installations(smothering or toxic effect) or an increased abundanceof few species close to source of contamination (organic

enrichment effect). Diversity shows a similar pattern tospecies richness with low diversity near installations andbackground levels being achieved by 2 km (Kingston,1992; Olsgard and Gray, 1995).A number of carrier fluids for invert emulsion drilling

fluids were assessed for their anaerobic biodegradabilityusing the standard European Centre for Ecotoxicologyand Toxicology of Chemicals (ECETOC) screening test(Steber and Herold, 1995). The extent of ultimate de-gradation of fatty acid esters I and II averaged (95% CL)82.5% (13.9) and 83.7% (13.1) over 35 days while oleylalcohol and 2-ethyl hexanol averaged 88.6% (14.8) and78.8% (21.4) degradation over 84 days. This contrastedwith degradation rates of only 3.9% (11.0) for mineraloil A over 35 days and 0.6% (16.2) for polyalphaolefin IIover 50 days (Steber and Herold, 1995). The authorsstated that anaerobic biodegradability was an essentialprerequisite for the prevention of long-term presenceand effects of drilling fluids in the marine environment.They found that fatty acid and alcohol-derived ester oilshad excellent biodegradability while mineral oils, dialkylethers, alpha-olefins, polyalphaolefins, linear alkylbenz-enes and an acetal derivative were only slowly biode-graded if at all. Overall the authors concluded that esteroils presently represented the only group of carrier fluidseasily accessible to anaerobic biodegradation.In another biodegradation study of drilling fluids, the

percentage ultimate biodegradation varied from 11% to85% for six drilling fluid mixtures assessed (Papp andWest, 1999). An internal olefin whole fluid (11%) and aparaffin whole fluid (18%) were the least biodegradabledrilling fluids and Biogreen BG5500 whole fluid (anoxygen-based fluid consisting of a fish oil ester) was themost biodegradable (85%). Integrated laboratory, mes-ocosm and field-scale tests for assessing environmentalimpact of non-water-based fluid (NWBF) discharges tothe marine environment are ‘‘being developed with in-dustry and scientific bodies’’ for this program in West-ern Australia.The sublethal effects of drilling fluids on 35 species of

marine organisms were reported in the earlier literature

Table 4

Acute toxicity of major Italian drilling fluid products (modified from Terzaghi et al., 1998)

Product type Acute toxicity EC50 Algae/LC50 (95% CL) brine shrimp (mg/l)

Algae (Phaeodacylum tricornutum) Brine shrimp

(Artemia salina)

Maximum concentration

in drilling fluids

Lignosulphonate 356 3953 (3972–4055) 23,000

Modified starch Not determined 10,000 17,000

Soltex asphalt 216 >10,000 17,000

XC-polymer >400 291 (250–335) 6000

Mor-rex maltodextrin Not determined >10,000 15,000

Carboxymethylcellulose (CMC) LV >10,000 >10,000 9000

Polyanionic cellulose (PAC) LV >10,000 >10,000 14,000

Wetting agent/detergent 65.4 341 (302–410) 800

Defoamer alcohol 9.15 5.41 (4.03–7.28) 1500

D.A. Holdway / Marine Pollution Bulletin 44 (2002) 185–203 191

(NRC, 1983 cited in Hinwood et al., 1994), all fluidstested being chromium or ferrochromium lignosulpho-nate fluids. Gulec (1994) investigated the effect of anester-based and a low salt PHPA mud on the buryingbehavior of the marine sand snail Polinices conicus. Hefound that the EC50 following 24 h of exposure variedfrom 21% to 27% for the suspended particulate phase(SPP) and from 23% to 38% for the liquid phase of esterdrilling mud; and from 26% to 33% for the SPP of thelow-salt PHPA mud. These relatively low toxicity’s fora sensitive behavioral test indicate that short-termsublethal effects of such drilling muds are of onlymoderate concern in the immediate vicinity of a drillingplatform.The potential impact of the SPP of drilling fluid on

seagrass was investigated using Thalassia testudinum andits epiphytes in concurrent 12-week laboratory and fieldstudies (Macauley et al., 1990). Test systems (both lab-oratory and field) were treated once per week to nominalconcentrations of 100 mg/l (ppm) SPP. Drilling fluidexposure had no significant effect on chlorophyll a or bcontent of Thalassia leaves. Epiphyte biomass on theleaves of Thalassia was temporarily reduced after sixweeks of SPP exposure but had recovered to controlvalues by 12 weeks of exposure. These results wouldindicate that chronic effects to marine sea grasses andtheir epiphytes from long-term exposure to drilling flu-ids do not appear to be likely to occur.Drilling fluid waste had modest inhibitory effects on

the growth rate of Staphylococcus and Pseudomonasspecies of soil bacterial isolates collected from a man-grove swamp location, but enhanced the growth rate ofAlcaligenes and Micrococcus species taken from thesame site (Benka-Coker and Olumagin, 1996). The au-thors speculated that the inhibitory effects of the drillingfluid might result in an accumulation of the waste in theenvironment though they also acknowledged that thestimulatory effects on other soil bacteria could offsetsuch impacts. Drilling fluids have also been shown toaffect the substrate specificity of marine bacteria withcontrols having lower overall variation in the percent-ages of heterotrophic bacterial subgroups (lipolytic,starch-hydrolyzing, proteolytic and cellulolytic bacteria)over the experimental period (28 days) than the drillingfluid exposed bacteria (Okpokwasili and Nnubia, 1995).Similar results were obtained for oil-spill dispersant-exposure. The authors conclude that the heterotrophicmicrobial processes were negatively affected by exposureto drilling fluids with a general trend of mild geomi-crobiological process inhibition in the marine environ-ment.Use of marine benthic community species diversity

and species dominance measurements combined withmultivariate analyses and ordination techniques per-mitted Gray et al. (1990) to distinguish site groupingsrelated to oil activities and in particular, to barium,

hydrocarbon and percentage of mud, at distances of upto 2–3 km from one source in the North Sea (Ekofisk)and up to 1.5 km from another North Sea source(Eldfisk). The first indications of changes in benthiccommunities were increased abundance patterns ofsome species and altered patterns of presence and ab-sence of rare species (Gray et al., 1990). This indicatesthat drilling fluids can have subtle and less easily iden-tified impacts much further away from platforms thanpreviously believed, but that high powered statisticaltechniques combined with well-designed sampling pro-grams are required to elucidate these effects.Even fewer studies have looked at the effects of

drilling fluids in the region within the first few meters ofthe seabed known as the benthic boundary layer (BBL).This region has specific characteristics which differ fromthe overlying water column and may result in particlessettling from the overlying water column remainingsuspended and concentrated within the BBL (Gordanet al., 1992; Muschenheim et al., 1995; Muschenheimand Milligan, 1996). In the recent laboratory studies ofsea scallops Placopecten magellanicus from GeorgesBank in the North Atlantic Ocean, simulation of thephysical conditions which exist in the BBL in the pres-ence of various components of drilling muds showedthat adult scallops had very low tolerance to suspendedclay. Concentrations as low as 0.5 mg/l (ppm) of barite,a major component on drilling fluids, caused significantdetrimental effects on adult scallop growth (Gordanet al., 1992). The authors conclude that on the basis ofinformation obtained thus far, a water quality standardfor the protection of scallop stocks will probably be lessthan 5 mg/l (ppm) for fine drilling wastes in the BBL.Recent studies of fine drilling waste particulates onthe Scotian Shelf in Canada have shown that transientretention of drilling wastes in the BBL can developover periods that are ecologically significant and thatthey may remain suspended in the BBL and be detect-able several kilometers from the discharge point(Muschenheim et al., 1995; Muschenheim and Milligan,1996).In another study, Georges Bank sea scallops (Placo-

pecten magellanicus) were exposed for two months toundiluted mineral oil-based drilling mud (OBM) cut-tings from two drilling platform sources Alma F-67 wellon the Scotian shelf off Nova Scotia and Terra Nova E-79 well on the Grand Banks off Newfoundland (Cran-ford and Gordon, 1991). Chronic mortality increasedfrom 12.5% in controls to 32% in scallops exposed toAlma-cuttings scallops, and 37.5% in scallops exposedto Terra Nova-cuttings. In surviving animals, cessationof reproductive and somatic tissue growth was observedalong with decreased body component condition indicesand failure of lipid reserve accumulation. This researchthus raised concerns regarding chronic impacts of ‘‘lowtoxicity’’ mineral OBM in the immediate vicinity of

192 D.A. Holdway / Marine Pollution Bulletin 44 (2002) 185–203

drilling platforms including mortality, growth and re-productive effects (Cranford and Gordon, 1991). Theauthors recognized the limitations of their labora-tory exposures in representing actual field exposureconditions, and noted that development of a high-energy exposure protocol to provide more ecologicallyrelevant sedimentary and current conditions was underway.In an important series of major field studies of

macrozoobenthic species exposed to discharges of oil-based cutting muds (OBM), water-based cutting muds(WBM) and ester-based cutting muds (EBM) in theNorth Sea, significant effects of both OBM and EBM onmacrobenthos species abundance were observed up to500 m or even 1000 m away from the drilling platformsources (Daan et al., 1990, 1994, 1995, 1996; Daan andMulder, 1994). Of particular interest was the lack ofsignificant WBM effects on the 15 species of macro-benthos that showed reduced abundance near OBMdischarge sites (Daan et al., 1994). A similar reductionin species abundance was found for EBM exposedmacrobenthos with some 12 species showing alteredabundance. Of these, one species, the opportunistpolychaete Capitella capitata, showed increased abun-dance near both OBM (Daan et al., 1994) and EBMsites (Daan et al., 1996) while all other indicator specieswere reduced near OBM and EBM sources. The authorsnoted the striking qualitative similarity between initialeffects related to exposure to OBM cutting dischargesand those resulting from exposure to EBM discharges.In particular, the abundances of the large individuals ofthe echinoderm Echinocardium cordatum and its symbi-ont, the bivalve mollusc Montacuta ferruginosa werereduced at the greatest distances from both OBM andEBM cutting sources. Stress is thought to relate to or-ganic enrichment with a reduction in the available ox-ygen in the sediment due to changes in both the physicaland chemical properties of the sediment. Increased ox-ygen consumption as a result of degradation is hy-pothesized as the most plausible explanation for EBMcutting discharges (Daan et al., 1996). The estimateddecay rate of the drilling mud esters indicated a meanhalf-life of 133 days with a lower confidence limit of 68days.Losses of low toxicity OBMs were recently estimated

to be 1297, 44 and 160 tonnes for the North Rankin Aplatform, Wanaea-6 well and Lynx-1A well on Austra-lia’s NorthWest shelf, respectively (Oliver and Fisher,1999). Analysis of species richness and abundance dataindicated that in the case of the North Rankin A plat-form, major acute effects occurred up to 400 m fromdischarge and that background was attained from 3000to 5000 m though the natural variability and poorsampling design made lower level effect determinationsomewhat uncertain. Analysis of the sediments andbiota at the Wanaea-3 well three years after completion

of drilling with water-based mud (WBM) demonstratedthat the effects of drilling could still be detected. Ele-vated levels of barium could be measured up to 200 mfrom the well head in all directions while lead was ele-vated up to 100 m in the direction of the prevailingcurrent. Species richness was lowest at the 5 m site fromthe well head relative to all other stations sampled threeyears after completion of drilling at Wanaea-6, biolog-ical effects appear to be limited to within 100 m of thecuttings discharge point with background levels of totalpetroleum hydrocarbons (TPH) and trace metals oc-curring near 1200 m in the direction of the prevailingcurrent (Oliver and Fisher, 1999).The toxicity of water-based drilling muds (WBM)

collected from an active platform off southern Californiato red abalone (H. rufescens) and brown cup corals(Paracyathus stearnsii) was assessed in the laboratory(Raimondi et al., 1997). This research indicated thateven low-toxicity water-based drilling muds might con-tribute to significant impacts on important processessuch as larval settlement in the case of abalone. Theyalso found that WBMs may have direct effects on sessileadult organisms typical of hard-bottom communities asindicated by the adult mortality, proportion of individ-uals showing tissue loss, and reduced relative viabilityobserved in brown cup corals (Raimondi et al., 1997).Their use of environmentally realistic test concentra-tions (range 0.002–200 mg/l) indicated that the effectsfound in the laboratory were of the same magnitude asthose likely to occur in the field.An excellent chronic concentration-response study

using winter flounder (Pleuronectes americanus) exposedfor 80 days to sediments enriched in aliphatic hydro-carbons from oil-base drill cuttings investigated physi-ological (condition indices and energy reserves),biochemical (mixed-function oxygenases (MFO)) andcellular (blood disorders and histopathology) biomar-kers of effect (Payne et al., 1995). With the exception of aslight MFO inhibition at the highest tested concentra-tion (1500 ppm TPH), there was no evidence of a con-centration-response and most indices remainedunaffected. These results thus failed to reject the nullhypothesis that there were no effects of the aliphaticcomponents of complex hydrocarbon mixtures such asOBMs on winter flounder, a surrogate for bottom-dwelling fish. It should be noted, however, that winterflounder do not feed in the winter and thus were not fedduring this experiment. Thus, these results pertain onlyto water-borne contaminants and not to potential up-take through food.In a flawed and limited study of growth rate of the

mud minnow Fundulus grandis exposed to mineral oil-based and synthetic liquid-based drilling muds, growthrates over 30 days were not significantly different be-tween treatments (Jones et al., 1991). There was someconfounding mortality due to water quality problems as

D.A. Holdway / Marine Pollution Bulletin 44 (2002) 185–203 193

well as poor growth rates in the controls, however, theresults are of limited value.

4. Crude oils

There is a very large but somewhat uneven literaturethat looks at the effects of crude oil on marine organismsand ecosystems. The vast majority of information looksat the effects on fish followed by marine invertebrateimpacts. This review will only look at the most recentliterature and the reader is directed to a number ofvarious reviews in this specific area (e.g., Volkman et al.,1994; NRC, 1985).

4.1. Acute toxicity of crude oils

There are a number of recent studies which have in-vestigated the acute toxicity of crude oil to aquatic or-ganisms (Table 5). While many of these acute toxicitystudies use the static-replacement bioassay approach(Gulec et al., 1997/1998; Gulec and Holdway, 1999,2000; Mitchell and Holdway, 2000; Fucik et al., 1995),the study by Moles (1998) provides acute toxicity in-formation based on flow-through test conditions. TPHconcentrations varied somewhat for each water accom-modated fraction (WAF) or water-soluble fraction(WSF). However, the overall acute toxicity betweenaquatic organisms generally only varied by about afactor of 5 from around 0.5 to 5 ppm TPH (Table 5). Interms of percentage WAF, this relates to somewherebetween 20% and 100%.It must be borne in mind that the method of pro-

ducing WAF or WSF will influence the actual TPH andPAH concentrations of the stock test solutions. Thiscan make direct comparisons of the literature valuessomewhat problematic, especially when combined withthe different specific chemical composition of each crudeoil.Freshwater invertebrates were only slightly more

sensitive than marine invertebrates (Mitchell andHoldway, 2000). Fish tend to be similar or slightly lesssensitive to crude oil than invertebrates (Gulec andHoldway, 2000; Moles, 1998; Fucik et al., 1995). It ishard to generalize about the toxicity of dispersed oilsince the type of dispersant can also affect the acutetoxicity of the resultant WAF. The main aspect is thatgreater amounts of TPH are put into the water columnthus causing greater acute toxicity to marine organisms.The relative toxicity in terms of actual TPH and PAHconcentrations appears to be only slightly to moderatelymore toxic, depending on the dispersant type used(Mitchell and Holdway, 2000; Gulec et al., 1997/1998;Gulec and Holdway, 1999, 2000).

The acute toxicity of burned oil WAF was found tobe significantly lower than for WAF or dispersed oilto both marine snails (P. conicus) and amphipods (All-orchestes compressa) compared to crude oil WAF anddispersed crude oil (Gulec and Holdway, 1999). Burnedoil residue mixture was not acutely toxic to the samespecies of amphipod and was only of very low toxicity tomarine snail behavior following acute exposure.

4.2. Chronic toxicity of crude oils

There is an increasing number of studies of the sub-lethal and chronic effects of crude oil on aquatic or-ganisms. This is because it is still uncertain whetherlong-term impacts of oil spills are a serious environ-mental hazard. Following the Exxon Valdez spill of 1989and other recent large-scale and high profile spills, andthe subsequent political and social concern, a great dealof research has been directed towards understanding thelong-term impacts on marine environments of exposureto crude oil (Botello et al., 1997; Burns et al., 1993;Lavering, 1994; Lee and Page, 1997; Lissner et al., 1991;Moore et al., 1997; Price, 1998; SEEEC, 1997; Silvaet al., 1997; Suchanek, 1993).Potential long-term effects on specific ecosystems

such as the Great Barrier Reef (Craik, 1991, Flood,1992), the North Sea (Ferm, 1996; Gray et al., 1999;McIntyre and Turnbull, 1992) or the Gulf of Mexico(Kennicutt et al., 1996a,b) are of concern and explora-tion, drilling and transport activities in these areas arebeing monitored and managed.Much of this research has been directed towards in-

vestigating the sub-lethal reproductive effects of crudeoil exposure to commercial species of fish includingherring and salmon. This section will review some of themost recent studies of chronic toxicity of crude oil andits constituents to aquatic organisms.A number of studies have found contaminated sedi-

ments, fish and invertebrates following an oil spill orlong-term chronic exposure to:

• crude oil (Alvarez Pineiro et al., 1996; Awad, 1995;Boehm et al., 1995; Burns and Knap, 1989; Boeer,1996; CSIRO, 1996; Fayad et al., 1996; Gajbhiyeet al., 1995; Gold-Bouchot et al., 1997; Sen Guptaet al., 1995; Irvine et al., 1999; Khan et al., 1995;Law et al., 1997; Massoud et al., 1998; Mille et al.,1998; Mohan and Prakash, 1998; Neff and Stubble-field, 1995; Nicodem et al., 1997; O’Clair et al.,1996; Sauer et al., 1998; Shang et al., 1997; Shortand Harris, 1996a,b; Shriadah, 1998; Venkateswaranand Tanaka, 1995)

or• PAHs (Anon., 1997; Hellou and Warren, 1997; Kan-ga et al., 1997; Kayal and Connell, 1995; Pereiraet al., 1996).

194 D.A. Holdway / Marine Pollution Bulletin 44 (2002) 185–203

Table 5

Acute toxicity of crude oil to aquatic organisms

Organism tested Crude oil Test conditions EC/LC50 (SE unless

indicated otherwise)

Reference

Marine amphipod

(Allorchestes compressa)

Bass Strait crude oil WAF

(�9 ppm TPH)96 h 60% static

replacement

31.1% (0.576) Gulec et al.

(1997/1998)

Marine amphipod

(Allorchestes compressa)

Dispersed Bass Strait crude oil

(100 ppm dispersed oil contains

�7 ppm TPH)

96 h 60% static

replacement

Corexit 9527: 16.2

ppm (2.8)

Gulec et al.

(1997/1998)

Corexit 9500: 14.8

ppm (0.8)

Marine amphipod

(Allorchestes compressa)

Burned Bass Strait crude oil

(burned oil WAF contained

�1.5 ppm TPH)

96 h 60% static

replacement

Burned oil WAF: 80%

(4.1)

Gulec and

Holdway (1999)

Burned oil residue:

>100% (–)

Marine snail

(Polinices conicus)

Bass Strait crude oil WAF

(�9 ppm TPH)30 min burying

behavior

19.0% (0.560) Gulec et al.

(1997/1998)

Marine snail

(Polinices conicus)

Dispersed Bass Strait crude oil

(100 ppm dispersed oil contains

�7 ppm TPH)

30 min burying

behavior

Corexit 9527: 65.4

ppm (2.0)

Gulec et al.

(1997/1998)

Corexit 9500: 56.3

ppm (1.9)

Marine snail

(Polinices conicus)

Burned Bass Strait crude oil

(burned oil WAF contained

�1.5 ppm TPH)

30 min burying

behavior

Burned oil WAF: no

effects

Gulec and

Holdway (1999)

Burned oil residue:

no effects

Ghost shrimp

(Palaemon serenus)

Bass Strait crude oil WAF

(�9 ppm TPH)96 h 50% static

replacement

25.8% (1.30) Gulec and

Holdway (2000)

Ghost shrimp

(Palaemon serenus)

Dispersed Bass Strait crude oil

(100 ppm dispersed oil contains

�7 ppm TPH)

96 h 50% static

replacement

Corexit 9527: 8.1

ppm (0.3)

Gulec and

Holdway (2000)

Corexit 9500: 3.6

ppm (0.3)

Larval Australian bass

(Macquaria novemaculeata)

Bass Strait crude oil WAF

(�9 ppm TPH)96 h 50% static

replacement

46.5% (1.60) Gulec and

Holdway (2000)

Larval Australian bass

(Macquaria novemaculeata)

Dispersed Bass Strait crude oil

(100 ppm dispersed oil contains

�7 ppm TPH)

96 h 50% static

replacement

Corexit 9527: 28.5

ppm (1.4)

Gulec and

Holdway (2000)

Corexit 9500: 14.1

ppm (2.6)

Green hydra

(Hydra viridissima)

Bass Strait crude oil WAF

(�1 ppm TPH stock solution)96 h 100% static

replacement

(freshwater)

0.7 ppm (0.1) Mitchell and

Holdway (2000)

Green hydra

(Hydra viridissima)

Dispersed Bass Strait crude oil

(20 ppm TPD Corexit 9527,

100 ppm TPH Corexit 9500)

96 h 100% static

replacement

(freshwater)

Corexit 9527: 9.0

ppm (0.5)

Mitchell and

Holdway (2000)

Corexit 9500: 7.2

ppm (0.1)

Pink salmon

(Oncorhynchus gorbuscha)

Cook Inlet Alaska crude oil WSF 96 h flow-through 1.2 ppm (0.2 CL)

total aromatic

hydrocarbons

Moles (1998)

Starry flounder

(Platichthys stellatus)

Cook Inlet Alaska crude oil WSF 96 h flow-through 1.8 ppm (0.2 CL)

total aromatic

hydrocarbons

Moles (1998)

Amphipod

(Boeckosimus hypsinotus)

Cook Inlet Alaska crude oil WSF 96 h flow-through >1.9 ppm total

aromatic hydrocarbons

Moles (1998)

Coonstripe shrimp

(Pandalus hypsinotus)

Cook Inlet Alaska crude oil WSF 96 h flow-through 1.4 ppm (0.2 CL)

total aromatic

hydrocarbons

Moles (1998)

King crab

(Paralithodes camtschaticus)

Cook Inlet Alaska crude oil WSF 96 h flow-through 1.5 ppm (0.3 CL)

total aromatic

hydrocarbons

Moles (1998)

Shore crab

(Hemigrapsus nudus)

Cook Inlet Alaska crude oil WSF 96 h flow-through >3.0 ppm total

aromatic hydrocarbons

Moles (1998)

Ocher starfish

(Evasterias troschelii)

Cook Inlet Alaska crude oil WSF 96 h flow-through >1.3 ppm totalaromatic hydrocarbons

Moles (1998)

Pink scallop

(Chlamys hericus)

Cook Inlet Alaska crude oil WSF 96 h flow-through 2.0 ppm (0.3 CL) total

aromatic hydrocarbons

Moles (1998)

File periwinkle

(Nucella lima)

Cook Inlet Alaska crude oil WSF 96 h flow-through >3.0 ppm total aromatic

hydrocarbons

Moles (1998)

(continued on next page)

D.A. Holdway / Marine Pollution Bulletin 44 (2002) 185–203 195

A variety of effects have been reported as a conse-quence of chronic oil exposure including:

• behavioral (Gulec and Holdway, 1999; Gulec et al.,1997/1998; Mackey and Hodgkinson, 1996; Moleset al., 1994; Temara et al., 1999; Wertheimer and Cel-ewycz, 1996),

• suppressed growth (Al-Yakoob et al., 1996; Gunder-sen et al., 1996; Mitchell and Holdway, 2000; Molesand Norcross, 1998),

• induced or inhibited enzyme systems and other molecu-lar effects (Anderson et al., 1999; Diaz-Mendez et al.,

1998; Gagnon and Holdway, 1999a,b; Gagnon andHoldway, 2000; George et al., 1994, 1995; Martyet al., 1997b; Readman et al., 1996; Stagg et al.,1995; Wheelock et al., 1999; Woodin et al., 1997),

• physiological responses (Alkindi et al., 1996; Antrimet al., 1995; Middaugh et al., 1998),

• reproductive (Beckman et al., 1995),• reduced immunity to disease and parasites (Moles,1999; Moles and Norcross, 1998),

• histopathological lesions and other cellular effects(Khan, 1995, 1998; Kocan et al., 1996; Marty et al.,1997a, 1999; Mortensen and Carls, 1994),

Table 5 (continued)

Organism tested Crude oil Test conditions EC/LC50 (SE unless

indicated otherwise)

Reference

Blue mussel

(Mytilus trossulus)

Cook Inlet Alaska crude oil WSF 96 h flow-through >3.0 ppm totalaromatic hydrocarbons

Moles

(1998)

Blue crab

(Callinectes sapidus)

Western Gulf of Mexico Oil WAF 96 h flow-through >100% (36% mortality

in 100% WAF

concentration)

Fucik et al.

(1995)

White shrimp

(Penaeus setiferus)

Western Gulf of Mexico Oil WAF 96 h flow-through >100% Fucik et al.

(1995)

Brown shrimp

(Penaeus aztecus)

Western Gulf of Mexico Oil WAF 96 h flow-through 59.9% Fucik et al.

(1995)

Blue crab

(Callinectes sapidus)

Central Gulf of Mexico Oil WAF 96 h flow-through 70.7% Fucik et al.

(1995)

White shrimp

(Penaeus setiferus)

Central Gulf of Mexico Oil WAF 96 h flow-through 30.2% Fucik et al.

(1995)

Eastern oyster

(Crassostrea virginica)

Dispersed Western Gulf of Mexico

Oil WAF

96 h static Corexit 9527 11.2 ppm (7.9–13.9 CL) Fucik et al.

(1995)

Eastern oyster

(Crassostrea virginica)

Dispersed Central Gulf of Mexico

Oil WAF

96 h static Corexit 9527 1.8 ppm (3.3–15.8 CL) Fucik et al.

(1995)

Inland silverside

(Menidia beryllina)

Western Gulf of Mexico Oil WAF 96 h flow-through 66.4% Fucik et al.

(1995)

Atlantic menhaden

(Brevoortia tyrannus)

Western Gulf of Mexico Oil WAF 48 h static 64.1% Fucik et al.

(1995)

Red drum

(Sciaenops ocellatus)

Western Gulf of Mexico Oil WAF 48 h static >100% Fucik et al.

(1995)

Spot

(Leiostomus xanthurus)

Western Gulf of Mexico Oil WAF 48 h static >100% Fucik et al.

(1995)

Inland silverside

(Menidia beryllina)

Central Gulf of Mexico Oil WAF 96 h flow-through 59.1% Fucik et al.

(1995)

Atlantic menhaden

(Brevoortia tyrannus)

Central Gulf of Mexico Oil WAF 48 h static 42.1% Fucik et al.

(1995)

Red drum

(Sciaenops ocellatus)

Central Gulf of Mexico Oil WAF 48 h static 74.0% Fucik et al.

(1995)

Spot

(Leiostomus xanthurus)

Central Gulf of Mexico Oil WAF 48 h static 70.7% Fucik et al.

(1995)

Blue crab

(Callinectes sapidus)

Dispersed Western Gulf of Mexico

Oil WAF

96 h flow-through

Corexit 9527

90.8 ppm Fucik et al.

(1995)

White shrimp

(Penaeus setiferus)

Dispersed Western Gulf of Mexico

Oil WAF

96 h flow-through

Corexit 9527

18.6 ppm Fucik et al.

(1995)

Brown shrimp

(Penaeus aztecus)

Dispersed Western Gulf of Mexico

Oil WAF

96 h flow-through

Corexit 9527

52.7 ppm Fucik et al.

(1995)

Blue crab

(Callinectes sapidus)

Dispersed Central Gulf of Mexico

Oil WAF

96 h flow-through

Corexit 9527

19.8 ppm Fucik et al.

(1995)

White shrimp

(Penaeus setiferus)

Dispersed Central Gulf of Mexico

Oil WAF

96 h flow-through

Corexit 9527

13.8 ppm Fucik et al.

(1995)

Pink salmon

(Oncorhynchus gorbusca)

Alaskan North Slope crude oil WSF 96 h flow-through 1.0, 2.2 and 2.8 ppm

for 1992, 1990 and 1991

juveniles, respectively

Birtwell et al.

(1999)

196 D.A. Holdway / Marine Pollution Bulletin 44 (2002) 185–203

• tainted flesh (Goodlad, 1996),• chronic mortality (Birtwell et al., 1999; Crump andEmson, 1998; Ewa-Oboho and Abby-Kalio, 1994; Fu-cik et al., 1995; Garrity et al., 1994; Moles, 1998), and

• reptile, bird and mammal impacts including the effectsof physical cleaning of oil (Attias et al., 1995; Conroyet al., 1997; Custer et al., 1994; CSIRO, 1999; Duffyet al., 1994; Feuston et al., 1997; Fowler et al., 1995;Hartung, 1995; Jenssen, 1996; Khan et al., 1996; Lips-comb et al., 1996;Mitchell, 1999; Schmidt, 1997; Stub-blefield et al., 1995; Vasquez et al., 1997; Wiens, 1996).

Middaugh et al. (1996) conducted a series of toxicity/teratogenicity tests on neutral fraction hydrocarbonsrecovered from sterile and biodegraded systems treatedwith weathered Alaska North Slope crude oil (ANS521). Embryonic inland silversides (Menidia beryllina)exposed to hydrocarbons from the sterile systems didnot have significant teratogenic responses at concentra-tions of 1%, 10%, and 100% (w/v) of WSFs.Silverside heartbeat was significantly lowered in days 5

and 6 of embryogenesis at the 100% sterile system WAF.TheWSF recovered from the 2- and 14-day stirred sterilesystems was 0.65 and 0.69 mg/l, respectively. In contrast,14 days of biodegradation resulted in 7.5 mg/l of neutralfraction hydrocarbons in 100% WAF and teratogenicresponses were found in embryonic inland silversidesexposed to 1%, 10% and 100% WSF from the biode-graded system. Heart contraction rates were reduced ondays 2–6 of embyogenesis at the 100% WSF concentra-tion compared to controls (Middaugh et al., 1996).The 1% biodegraded WSF thus corresponded to a

concentration of only 0.075 mg/l of neutral fractionhydrocarbons which caused significant teratogenic ef-fects in inland silverside. The authors conclude fromtheir results and those of earlier studies that severalmechanisms may be involved in the toxicity of crude oilto embryonic, larval and adult fishes.The proposedmechanisms (Middaugh et al., 1996) are:

• ovarian toxicity from direct uptake and sequesteringin ovary of low molecular weight WSF;

• embryonic toxicity or teratogenic effects from directcontact with oil;

• increases in WSF from use of dispersants;• increases in the WSF of higher molecular weight neu-tral oil fractions through biodegradation and bio-emulsification of weathered crude oil;

• bioaccumulation in larval fishes of WSF through pre-dation on contaminated invertebrate zooplankters;

• bioaccumulation of oil in larval and juvenile fishthrough direct dermal contact, uptake of WSF fromwater or by direct ingestion.

One study, however, indicated that oil exposure fromtheExxon Valdez oil spill ofMarch 1989 posed only a low

level of risk to pink salmon (Oncorhynchus gorbuscha) inPrince William Sound as a consequence of: low concen-trations of petroleum that actually entered the watercolumn; the limited number of streams actually oiled; andthe flushing of the intertidal incubation areas of thosestreams (Brannon andMaki, 1996). There is also evidencethat in areas of natural oil seepage, oil in seawater is notnecessarily bad for the environment (Schneider, 1995).

5. Other effects

There are a variety of other effects that have beenreported in relation to offshore oil and gas productionon both temperate and tropical marine ecological pro-cesses. One major area of potential impact is from themetals, which are associated with the drilling muds (seeSection 3). There is a whole literature associated withthe impact of metals on marine organisms and thereader is directed to this as this exceeds the scope of thisreview. Recent studies have confirmed that metals canbe an important issue of environmental concern owingtheir presence in crude oil (Dekkers and Daane, 1999)and in marine sediments around oil and gas productionfacilities (Kennicutt et al., 1996a,b). Their ability tobioaccumulate in tissues and in some cases, biomagnifyup food webs makes them potential contaminants ofsignificance (Al-Muzaini and Jacob, 1996; Andersonet al., 1997; Daffa, 1996; Gulec, 1994; Plasman, 1998).Sediment contamination levels appear to correlate wellwith reduced diversity and increased toxicity to aquaticorganisms (Gulec, 1994; Hartwell et al., 1998).One metal that appears to often be elevated around

drilling platforms is barium (Ba), where residual excessBa has been reported up to an order of magnitude abovebackground within 500 m of offshore oil and gas plat-forms in the Santa Marie Basin, CA, USA (Phillips et al.,1998). Sediment increases in Ba represented 6–11% ofthe total Ba discharged during the two drilling periodsincluded in the analysis and the elevated levels werelikely associated with cutting particles (rock chippings)deposited near the base of the platforms (Phillips et al.,1998). Barite (BaSO4) is a naturally occurring densemineral and is a major component of almost all drillingmuds (see Section 3). Barium concentrations in thesediment have thus been frequently used as a tracer tomonitor offshore oil and gas discharges (Hartley, 1996;Phillips et al., 1998). Recent work has shown that cau-tion needs to be used in this application owing to thelarge variations (2–3 orders of magnitude) in measuredBa concentrations possible depending on the extractionmethod used (Hartley, 1996).Another aspect associated with offshore oil and gas

production is the initial offshore seismic exploration thatprecedes development and the potential impacts of such

D.A. Holdway / Marine Pollution Bulletin 44 (2002) 185–203 197

activities on marine ecosystems. Although this area ofresearch is outside of the scope of this review, there is asignificant literature in the area, and recent studies havefocussed on biochemical responses to stress induced bysuch seismic prospecting using air gun acoustic waves(Santulli et al., 1999). With respect to European sea bass(Dicentrarchus labrax L.), the effects were transitory innature and there was a rapid (<72 h) recovery of ho-meostasis after acoustic stress with no observed mor-tality (Santulli et al., 1999).

6. Suspected but unconfirmed impacts on tropical and

temperate marine systems and further studies required to

clarify those impacts

One area where further research is required involvesthe potential impacts of PFW on early developmentstages of marine invertebrates including the criticalprocesses of metamorphosis and settling behavior. Oneof the most intriguing possibilities raised by this reviewis the hypothesis of Krause et al. (1992) that all of theobserved PFW effects could be mediated through asingle unifying toxicological mechanism involving mi-crotubule-mediated effects. It is rare in applied sciencesuch as ecotoxicology for such unifying theories to beproposed although some progress has been made in thestudy of quantitative structure activity relationships(QSAR) of chemicals involving like modes of action.Designing experiments to critically test this proposed

unifying hypothesis would appear to be a very usefuland specific area of future research to pursue.Other areas requiring further research include the

study of the ecological significance of PFW effects onzooplankton in the surfacemicrolayer, particularly effectson embryo and larval fish survival. Equally of interest,but in the completely opposite physical direction, are theeffects of suspended drilling fluid particles in the BBL, aregion of dynamic energy inmany parts of the world. Thisreview indicated that long-term impacts might be occur-ring in both of these zones but that studies to date werelimited in their scale and their conclusions were uncer-tain relative to their environmental significance.Other areas of potential impacts of offshore oil and

gas production wastes include long-term impacts onmarine populations as a consequence of low-level butchronic exposure to petroleum hydrocarbons, drillingfluids, metals and other chemicals associated with theindustrial activity.Generally, the temporal and spatial scales of these

studies, along with the large levels of inherent variationin natural environments, have precluded our abilityto predict the potential long-term environmental im-pacts of the offshore oil and gas production industry. Aseries of critical questions regarding the environmental

effects of the offshore oil and gas production industrystill remain unanswered and are listed below:

• What impact do the relatively short-term activities ofthe offshore oil and gas production industry have onthe long-term sustainability of the marine environ-ment?

• Are the impacts on the structure and density of ben-thic communities observed in the immediate vicinityof many oil and gas platforms of any significance tothe long-term productivity and community diversityof the marine ecosystems involved?

• What are the impacts 10, 20 and 30 years followingthe commencement of oil and gas production?

• What are the impacts 10, 20 and 30 years followingthe cessation of oil and gas production?

• What is the potential of oil and gas production wastesto be causing unknown effects as a consequence of de-layed toxicity mechanisms such as endocrine disrup-tion or the slow increase in background toxic metals?

• Can biomarkers of exposure and effects be used tomonitor for significant short-term and long-term im-pacts of oil and gas production wastes?

• What are the relative risks of environmental impactfrom the oil and gas production industry comparedto other important threats to marine ecosystems?

Such threats would include introduced alien species,altered marine habitat (e.g., loss of sea grass beds,dredging, coastal development), and the overall increasein the loading of various urban wastes from non-discretesources as a consequence of rapidly increasing popula-tion?With global scale challenges such as climate change,

ozone depletion, resource depletion and long-rangetransport of persistent atmospheric pollutants, deter-mining the long-term environmental significance of ac-tivities such as oil and gas production in isolation, andwithout ensuring appropriate temporal and spatialscales, is extremely challenging if not impossible. Themain areas of research required appear to involve highquality long-term studies of chronic impacts on wholepopulations, communities and even ecosystems. Use ofproperly designed monitoring programs and appropri-ate statistical analyses can assist in answering many ofthese questions, provided that the studies are designedaround the questions to be asked and not the other wayaround. Often this requires the long-term commitmentof resources on a temporal scale rarely achieved by in-dustry or governments whose goals and objectives aregenerally of a much shorter time frame.Thus, committing funds for ecological process studies

to be undertaken over 10–20 years is a very difficult task.However, without this type of approach, many of themost important questions regarding the long-term en-vironmental sustainability of the industry can simply not

198 D.A. Holdway / Marine Pollution Bulletin 44 (2002) 185–203

be addressed with any confidence. Although much valuecan be obtained from a variety of short-term experi-ments, it is generally not possible in the laboratory toinvestigate and understand the responses of whole eco-systems over the actual time and spatial scales involved.Reductionism will never fully describe complex biolog-ical ecosystems because the whole always exceeds thesum of the individual parts. It is thus essential that moreholistic research paradigms be employed to understandecosystem impacts.

Acknowledgements

I would like to thank Ms Linda Worland of theMarine Biological Research Institute of Japan for ini-tiating the process of undertaking the review and as-sisting in all of the processes involved. I thank Ms KellyRyder for collecting and collating the literature used inthis review, Professor Peter Coloe for providing the re-sources of the Department of Applied Biology andBiotechnology to support my undertaking this task, andMr Takeshi Yamaguchi of the Safety and EnvironmentCentre for Petroleum Development Japan for approvinga contract to undertake this review.

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