lable at ScienceDirect

Environmental Pollution 158 (2010) 1809–1816

Contents lists avai

Environmental Pollution

journal homepage: www.elsevier .com/locate/envpol

Environmental and human health risk assessment of organic micro-pollutantsoccurring in a Spanish marine fish farm

Ivan Munoz*, Marıa J. Martınez Bueno, Ana Aguera, Amadeo R. Fernandez-AlbaDepartamento de Hidrogeologıa y Quımica Analıtica, Universidad de Almerıa, 04120 Almerıa, Spain

Exposure and effects of twelve organic micro-pollutants are evaluated

at a Spanish fish farm.

a r t i c l e i n f o

Article history:Received 14 May 2009Received in revised form30 September 2009Accepted 5 November 2009

Keywords:AquacultureEcological risk assessmentHealth risk assessmentSecondary poisoningIrgarol 1051

* Corresponding author. Tel.: þ34 950014139; fax:E-mail addresses: ivanmuno@ual.es (I. Munoz), m

Bueno), aaguera@ual.es (A. Aguera), amadeo@ual.es (

0269-7491/$ – see front matter � 2009 Elsevier Ltd.doi:10.1016/j.envpol.2009.11.006

a b s t r a c t

In this work the risk posed to seawater organisms, predators and humans is assessed, as a consequence ofexposure to 12 organic micro-pollutants, namely metronidazole, trimethoprim, erythromycin, simazine,flumequine, carbaryl, atrazine, diuron, terbutryn, irgarol, diphenyl sulphone (DPS) and 2-thio-cyanomethylthiobenzothiazole (TCMTB). The risk assessment study is based on a 1-year monitoringstudy at a Spanish marine fish farm, involving passive sampling techniques. The results showed that therisk threshold for irgarol concerning seawater organisms is exceeded. On the other hand, the risk topredators and especially humans through consumption of fish is very low, due to the low bio-concentration potential of the substances assessed.

� 2009 Elsevier Ltd. All rights reserved.

1. Introduction

Aquaculture is the farming of aquatic organisms including fish,molluscs, crustaceans and aquatic plants, using techniquesdesigned to increase the productivity of these organisms beyondthe natural capacity of the environment. Intensive aquaculture iscommonly practised in cages or ponds: involving the control ofbreeding, and supply of artificial feed and medication. The increasein demand for seafood and the decline in world fisheries havecontributed to an unprecedented growth in this industry overrecent decades. As a result, it is growing more rapidly than anyother animal food-producing sector in the world (Nierentz, 2007).Aquaculture production in 2005 (excluding plants) was reported asbeing 48.1 million tonnes, which represents 45% of the globalseafood supply and is valued at 70.9 US$ billion in value (Nierentz,2007). Unfortunately, the sustainability of intensive aquaculturehas been brought into question, due to its potential environmentalimpacts, including pressure on feed resources (Naylor et al., 2000),destruction of mangroves and wetlands (Paez-Osuna, 2001),discharge of particulate and dissolved organic matter throughfaeces and feed wastage (Read and Fernandes, 2003), eutrophica-tion (Folke et al., 1994; Loya et al., 2004), genetic interaction

þ34 950015483.jbueno@ual.es (M.J. MartınezA.R. Fernandez-Alba).

All rights reserved.

between escaped and wild fish (Youngson et al., 2001), diseasetransfer to wild fish (Heggberget et al., 1993) and human healthrisks due to accumulation of persistent organic pollutants in farmedfish (Hites et al., 2004). Another key impact of intensive aquacultureis the dispersion of chemicals in the environment (Graslund andBengtsson, 2001), such as disinfectants, antifoulants and veterinarymedicines. These chemicals are essential for aquaculture in order toincrease and control production of seed in hatcheries, increasefeeding efficiency, improve survival rates, control pathogens anddiseases and reduce transport stress (Huntington et al., 2006).However, the aquaculture industry has adopted the use of chem-icals originally developed for other sectors, especially agriculture.Many chemicals now in common use in aquaculture have neverbeen evaluated in the context of their effects on the aquatic envi-ronment, particularly coastal waters (Huntington et al., 2006). Oneof the reasons for this is the lack of reliable analytical data inseawater, as a consequence of the difficulties in detecting organicpollutants in this medium, such as the complexity of the matrix, thehigh dilution factor or degradation phenomena (Pouliquen et al.,2007). For this reason, the environmental assessment of chemicalsin the marine environment requires the development of highly-specific and sensitive analytical procedures, allowing us to detectpollutant concentrations below ng L�1 or pg L�1.

From October 2005 to October 2006 a micro-pollutant moni-toring campaign was carried out in a fish farm located in south-eastern Spain, where sea bream (Sparus aurata) and sea bass(Dicentrarchus labrax) are farmed. Instead of traditional water

Table 1Analytical results obtained during a 1-year monitoring campaign at the fish farm.

Group Compound Positivesamples(n ¼ 12)a

Concentrationrange in positivesamples (ng L�1)a

PECseaw

(ng L�1)b

Antibiotics Ciprofloxacin n.d – –Enrofloxacin n.d – –Erythromycin 5 0.01–0.03 0.0073Flumequine 1 0.13 0.011Mepivacaine n.d – –Metronidazole 1 13.4 1.12Oxolinic acid n.d – –Oxytetracycline n.d – –Sulfamethoxazole n.d – –Tetracycline n.d – –Trimethoprim 1 0.23 0.02

Herbicides Albendazole n.d – –Atrazine 12 0.2–1.5 0.85Carbaryl 1 4.50 0.38Dichlorvos n.d – –Diflubenzuron n.d – –Diphenyl sulphone,DPS

12 15.5–75.6 45.55

Diuron 5 0.4–2.5 1.45Simazine 12 0.1–0.9 0.95Terbutryn 10 0.02–0.1 0.06

Fungicides Malachite green n.d – –

Biocides Irgarol 12 0.02–0.7 0.36TCMTB 1 3.10 0.26

n.d.: not detected.a Martınez-Bueno et al. (2009).b Calculated as a yearly average. Zero was used as the concentration in samples

were the compound was not detected.

I. Munoz et al. / Environmental Pollution 158 (2010) 1809–18161810

sampling methods, passive sampling methods were used, namelyPolar Organic Chemical Integrative Samplers (POCIS) (Alvarez et al.,2004). Target substances included 23 organic chemicals belongingto different groups: antibiotics, fungicides, herbicides and biocides.It must be stressed that the particular products used in the farmwere not disclosed by the company. Hence, the target substanceswere selected on the basis of being commonly used in aquaculture.12 substances were detected during the one-year campaign:metronidazole, trimethoprim, erythromycin, simazine, flumequine,carbaryl, atrazine, diuron, terbutryn, irgarol, diphenyl sulphone(DPS) and 2-thiocyanomethylthiobenzothiazole (TCMTB). In thispaper we assess by means of Risk Assessment the toxicologicalrisks to the marine aquatic environment and to human healthposed by these chemicals. Further details on the micro-pollutantmonitoring campaign can be found in Martınez-Bueno et al. (2009).

2. Risk assessment methodology

The Risk Assessment of chemicals has been carried out using the EuropeanCommission’s Technical Guidance Document on Risk Assessment (TGDRA) (EC,2003) as the methodological reference.

2.1. Protection goals

Risks addressed by this paper are those related to toxic effects in the environmentand in humans. The areas of protection for which risk is assessed are the following:

-Seawater organisms-Seawater (fish-eating) predators-Humans, through fish consumption

Protecting marine sediment-dwelling organisms is also relevant in this context;however, the monitoring campaign in the fish farm did not include sedimentanalyses. In addition, experimental toxicity data on sediment organisms is scarce.For this reason, the environmental risk on sediments is only discussed qualitatively.

2.2. Target substances

The substances subject to the risk assessment are those which were detected inthe monitoring campaign (Table 1). All these substances are assessed in terms of riskto seawater organisms, predators and humans upon consumption of fishery prod-ucts. It must be highlighted that the actual chemicals used in the farm were notdisclosed. Therefore, the list of target pollutants could be incomplete.

2.3. Exposure assessment

The goal of the exposure assessment is to estimate the predicted environmentalconcentrations or doses to which organisms in ecosystems and humans will beexposed. The assessment is based on the calculations proposed by the TGDRA(European Commission, 2003) and the European Uniform System for the Evaluationof Substances (EUSES) (European Commission, 2004).

Predicted environmental concentrations in seawater (PECseaw, in mg L�1) havebeen obtained from the analytical results of the monitoring campaign (Table 1).PECseaw corresponds to the yearly average concentration, calculated as the averagefrom the 12 samples. When a substance was not detected in a sample, theconcentration taken into account for that sample was zero.

The predicted concentration in fish (Cfish, in mg kgwwt�1 ) is calculated following

the TGDRA guidelines, using eq. (1):

Cfish ¼ PECseaw � BCFfish � BMFfish (1)

where BCFfish is the bioconcentration factor in fish (L kgwwt�1 ) and BMFfish is the

biomagnification factor in fish (dimensionless). Values for BCFfish (Table 2) have beenobtained from published experimental measures, or in the absence of the latter, bymeans of the BCFWIN program (Meylan et al., 1999). BMFfish has been estimatedusing the semi-quantitative approach suggested in the TGDRA (part II, Table 21),which assigns values in the 1–10 range, based on the magnitudes of log Kow andBCFfish. For all the substances in our case study, the obtained BMFfish is 1.

The predicted human dose via consumption of farmed fish (PHD, in mgkgbw�1 d�1) is calculated using eq. (2):

PHD ¼ Cfish � IHfish

BW(2)

where IHfish is the fish intake (kg person�1 d�1) and BW is the body weight, assumedto be 70 kg (European Commission, 2004). The average finfish consumption in Spain

(including fresh, frozen and canned fish) is 0.07 kg person�1 d�1 (Ministerio deAgricultura, Pesca y Alimentacion, 2006). Using eq. (2), with the data mentionedconstitutes a worst-case approach, since it is assumed that the consumer’s wholefinfish diet consists of sea bass/sea bream, and that the latter originates exclusivelyfrom the studied farm. In Table 3 the predicted concentrations and doses calculatedwith eqs. (1) and (2) are summarised.

2.4. Effects assessment

Effects assessment concerns the hazard identification and dose-responseassessment of toxicological and ecotoxicological data. In ecotoxicological effectsassessment, the predicted no-effect concentrations (PNECs) are derived fromexperimental toxicity data using assessment factors. In human toxicological effectsassessment, a human reference dose (HRD) is derived from the available data.

The predicted no-effect concentration for seawater organisms (PNECseaw) hasbeen obtained for most substances by means of single-species ecotoxicity data fromtests with seawater and/or freshwater organisms, and the application of assessmentfactors. Most of the references used for aquatic ecotoxicity, either from seawater orfreshwater, were retrieved from the USEPA Ecotox database (USEPA, 2009a),although in the particular case of DPS – due to the lack of experimental toxicityvalues to complete the minimum dataset (fish, crustaceans and algae) – values fromthe ECOSAR software were used (USEPA, 2009b). Concerning assessment factors,these were chosen depending on the number and the quality of the ecotoxicity dataavailable, as suggested by the TGDRA (part II, Table 25).

On the other hand, the pesticides simazine, atrazine and diuron are prioritysubstances classified in the European Water Framework Directive (EuropeanParliament, 2000), for which environmental quality standards (EQS) have recentlybeen approved through the Directive on Priority Substances (European Parliament,2008). For these three substances, the corresponding EQS have been used asPNECseaw, since they were determined following risk assessment methods andaccording to the Water Framework Directive EQS applied for coastal waters.

Concerning secondary poisoning, the concentration of chemicals in food forpredators should be below the predicted no-effect concentration for predators(PNECoral) in a (sub)chronic dietary toxicity test with animals representative of fish-eating birds or mammals. PNECoral is calculated from a non-observed effectconcentration (NOEC) in food and assessment factors are set by the TGDRA (part II,Table 23). In the absence of a NOEC, the non-observed effect level (NOAEL) formammals or birds can be converted into a NOEC in food by means of appropriateconversion factors provided by the TGDRA (part II, eqs. 77 and 78). For metroni-dazole, trimethoprim, erythromycin and DPS, it was not possible to find NOEC or

Table 2Log Kow, BCF and toxicity data for predators and humans.

Substance Log Kowa BCF (L kgwwt�1 ) Toxicity in mammals/birds Toxicity in humans

Value Source PNECoral

(mg kgfood�1 )

Source HRD(mg kgbw

�1 d�1)Source

Metronidazole �0.02 3.162 BCFWINb 1 Estimated from an oral LD50 in rat of 3000 mg kgbw�1 (ChemIDplusc), an

assessment factor of 2000 to obtain a NOAEL (Layton et al., 1987),a conversion factor to NOEC of 20 kgbw d kgfood

�1 for rat (TGDRAd) and anassessment factor to PNECoral of 30 (TGDRAe)

0.03 Estimated from an oral LD50in rat of 3000 mg kgbw

�1

(ChemIDplusc) and anassessment factor of 105

(Layton et al., 1987)Trimethoprim 0.91 3.162 BCFWINb 0.38 Estimated from an oral LD50 in mouse of 2800 mg kgbw

�1 (ChemIDplusc), anassessment factor of 2000 to obtain a NOAEL (Layton et al., 1987),a conversion factor to NOEC of 8.3 kgbw d kgfood

�1 for mouse (TGDRAd), and anassessment factor to PNECoral of 30 (TGDRAe)

0.0094 ADI (Cunninghamet al., 2009)

Erythromycin 3.06 45.31 BCFWINb 1.5 Estimated from an oral LD50 in rat of 4600 mg kgbw�1 (ChemIDplusc), an

assessment factor of 2000 to obtain a NOAEL (Layton et al., 1987),a conversion factor to NOEC of 20 kgbw d kgfood

�1 for rat (TGDRAd), and anassessment factor to PNECoral of 30 (TGDRAe)

0.04 ADI (Schwab et al., 2005)

Simazine 2.20 1 EC (2005a) 0.33 Based on a NOEC in rat, 2-year feeding study (USEPA., 2009c), and anassessment factor of 30 (TGDRAe)

0.005 ADI (EC, 2005a)

Flumequine 1.60 3.162 BCFWINb 2.3 Estimated from an oral NOEL in mouse of 25 mg kgbw�1 d�1 (JECFA, 2004),

a conversion factor to NOEC of 8.3 kgbw d kgfood�1 for mouse (TGDRAd), and an

assessment factor to PNECoral of 90 (TGDRAe)

0.03 ADI (JECFA, 2004)

Carbaryl 2.36 9 Kanazawa (1980) 6.7 Based on a NOEC from rat chronic feeding study (USEPA., 2009c) and anassessment factor to PNECoral of 30 (TGDRAe)

0.1 RfD (USEPA., 2009c)

Atrazine 2.61 12 EC (2005b) 7.5 Based on a NOEC from reproductive toxicity testing in mallard duck andbobwhite quail (EC, 2005b) and an assessment factor to PNECoral of 30(TGDRAe)

0.005 ADI (EC, 2005b)

Diuron 2.68 2 EC (2005c) 0.83 Based on a NOEC from a 2-year dog feeding study (USEPA., 2009c) and anassessment factor of 30 (TGDRAe)

0.007 ADI (EC, 2005c)

Terbutryn 3.74 72.4 PPDB (2009) 0.066 Based on a NOEC in rat, 2-year feeding study (USEPA., 2009c) and anassessment factor of 30 (TGDRAe)

0.001 RfD (USEPA., 2009c)

Irgarol 3.95 160 Ciba Specialty ChemicalsCorporation (2005)

2.2 Based on a NOEL in rat (90-day feeding study) of 9.7 mg kgbw�1 d�1(JECFA,

2004), a conversion factor to NOEC of 20 kgbw d kgfood�1 for rat (TGDRAd) and

an assessment factor to PNECoral of 90 (TGDRAe)

0.097 Based on a NOEL of 9.7 mg kgbw�1

from a 90-day subchronicoral toxicity in Rats(Ciba Specialty ChemicalsCorporation, 2005) andan assessment factor of100 (Falk-Filipsson et al., 2007)

DPS 2.40 14 BCFWINb 0.052 Estimated from an oral LD50 in mouse of 375 mg kgbw�1 (ChemIDplusc), an

assessment factor of 2000 to obtain a NOAEL (Layton et al., 1987)a conversion factor to NOEC of 8.3 kgbw d kgfood

�1 for mouse (TGDRAd) and anassessment factor to PNECoral of 30 (TGDRAe)

0.00375 Estimated from an oralLD50 in mouse of 375 mg kgbw

�1

(ChemIDplusc) and anassessment factor of105 (Layton et al., 1987)

TCMTB 3.30 69.34 BCFWINb 1.5 Based on a 8-day LC50, avian acute dietary test with bobwhite quail (USEPA,2006) and an assessment factor to PNECoral of 3000 (TGDRAe)

0.013 RfD (USEPA, 2006)

a Sources: Siracuse Research Corporation (2009), except Irgarol, from Sakkas et al. (2002).b Meylan et al. (1999).c U.S. National Library of Medicine (2009).d Table 22 in the TGDRA, part II (p. 129).e Table 23 in the TGDRA, part II (p. 130).

I.Mun oz

etal./

Environmental

Pollution158

(2010)1809–1816

1811

Table 3Predicted environmental concentrations in fish (Cfish) and predicted human doses(PHD).

Substance Cfish (mg kgwwt�1 ) PHD (mg kgbw

�1 d�1)

Metronidazole 3.5 � 10�6 3.5 � 10�9

Trimethoprim 6.3 � 10�8 6.3 � 10�11

Erythromycin 3.3 � 10�7 3.3 � 10�10

Simazine 9.5 � 10�7 9.5 � 10�10

Flumequine 3.5 � 10�8 3.5 � 10�11

Carbaryl 3.4 � 10�6 3.4 � 10�9

Atrazine 1.0 � 10�5 1.0 � 10�8

Diuron 9.6 � 10�7 9.6 � 10�10

Terbutryn 2.9 � 10�6 2.9 � 10�9

Irgarol 5.8 � 10�5 5.8 � 10�8

DPS 6.4 � 10�4 6.4 � 10�7

TCMTB 1.8 � 10�5 1.8 � 10�8

I. Munoz et al. / Environmental Pollution 158 (2010) 1809–18161812

NOAEL values for birds or mammals. In order to include these substances in theassessment of secondary poisoning, NOAEL values were estimated using dietaryhalf-maximal lethal doses (LD50) from mammals, available in the ChemIDplusAdvanced Database (U.S. National Library of Medicine, 2009) and by using anassessment factor of 2000 (Layton et al., 1987).

The HRD refers in this study to a toxicity threshold for humans, representing themaximum oral intake values for which long-term adverse effects are not expected.When these thresholds were available, in the form of, for example, acceptable dailyintakes (ADI) from the Joint FAO/WHO Expert Committee on Food Additives, orReference Doses (RfD) from the USEPA IRIS database (USEPA, 2009c), they wereused. When the above values were not available, NOAEL values from oral exposure inmammals were used instead. In this case, an assessment factor was applied toaccount for uncertainty related to inter-species variability, human variation insensitivity, etc. In order to derive a HRD from NOAEL, an assessment factor of 100was used (Falk-Filipsson et al., 2007). For metronidazole and DPS, no NOAEL valueswere found. In order to include these substances in the human toxicity assessment,HRD was estimated using oral LD50 values from mammals, available in the Chem-IDplus Advanced Database (U.S. National Library of Medicine, 2009) and anassessment factor of 105 (Layton et al., 1987). In Tables 2 and 4, the detailed data usedin the effects assessment is shown.

2.5. Risk characterisation

Risk Characterisation Ratios (RCR) are derived for the three areas of protection,by comparing exposure levels to suitable no-effect levels. For the environmentalareas of protection, RCR is calculated with eqs. (3) and (4):

RCRseaw ¼PECseaw

PNECseaw(3)

RCRpred ¼Cfish

PNECoral(4)

For human toxicity the ratio of PHD to HRD is used (eq. (5)):

RCRhuman ¼PHDHRD

(5)

A RCR below 1 means that adverse effects are not expected for the corre-sponding substance and area of protection, whereas a value above 1 means thatadverse effects are likely to occur, thus calling for risk reduction measures.

3. Results and discussion

The results of the risk characterisation step are shown in Fig. 1,where each graphic corresponds to one protection goal: seawaterorganisms, predators and humans. It can be seen that, with theexception of the antifouling irgarol, none of the assessedsubstances pose a substantial risk to any of the three protectiongoals. In seawater ecotoxicity it can be seen that the RCRseaw forirgarol is 1.8, and therefore above the adverse-effects threshold.Concerning the risk to predators, the highest RCRpred belongs toDPS (0.01), while the remaining substances are several orders ofmagnitude below. Finally, the risk to humans is even lower thanthat found for predators; the highest RCRhuman is 0.0002, corre-sponding to a margin of exposure of 5000.

3.1. Concentrations in seawater

The concentration of pollutants in seawater is very low, as canbe seen in Table 1. Actually only 12 out of 23 target pollutants weredetected, and from these 12, only 4 were detected in all samples.Unfortunately there are not many studies on organic micro-pollutants in seawater for this region. Piedra et al. (2000) carriedout an 8-month monitoring study of three marinas in this area,reporting concentrations of 50–1000 ng L�1 and 40–800 ng L�1 forirgarol and diuron, respectively; whereas TCMTB was detected onlyoccasionally at concentrations below 10 ng L�1. Even though thetarget pollutants are used in aquaculture, they may also come fromother sources apart from marinas, in particular from wastewaterdischarges. In an 11-month monitoring study of a local wastewatertreatment plant discharge, average concentrations of metronida-zole (76 ng L�1), trimethoprim (410 ng L�1), erythromycin(640 ng L�1), simazine (94 ng L�1), atrazine (96 ng L�1) and diuron(510 ng L�1) were determined (Munoz et al., 2008). Since the fishfarm is located at a distance of 2 km from one the above-mentionedmarinas, and to a city with a population of 77 000 inhabitants, theactual contribution of the farm to the detected levels of pollution isof an unknown extent, since these levels could be backgroundconcentrations from nearby activities, after dilution, transport anddegradation.

3.2. Risk to seawater organisms

In terms of potential risk, the most outstanding result from thiscase study is the impact of irgarol on seawater organisms. Thissubstance is used in mariculture devices such as nets, and on boathulls, in order to prevent biofouling. Irgarol was promoted in themid-1980s as an alternative biocide after the banning of tributyltin(TBT) (Morley et al., 2003). Nevertheless, the use of irgarol itself hasalso been recently restricted in some countries like Sweden,Denmark and the UK (Konstantinou and Albanis, 2004).

As can be seen in Table 1, this substance was one of the fewfound in all the samples analysed during the campaign, withconcentrations ranging from 0.02 to 0.7 ng L�1. The key to theidentified risk of irgarol is the specific mode of action of thissubstance, which is a powerful inhibitor of photosynthesis. This canbe seen in Table 4, where the lowest toxicity thresholds are thosefor primary producers: the diatoms Skeletonema costatum (NOEC10 ng L�1) and Navicula pelliculosa (EC50 100 ng L�1) and themacrophyte Zostera marina (EC50 200 ng L�1). NOEC values for thissubstance have been reported in studies involving phytoplanktoncommunities and mesocosm studies as 15.7 ng L�1 (0.062 nM, Dahland Blanck, 1996) and 8–80 ng L�1 (Nystrom et al., 2002). Theresulting PNECseaw of 0.2 ng L�1 for irgarol in our study is lowerthan others found in the literature: Thomas et al. (2001) deter-mined a PNECseaw of 25 ng L�1, based on ecotoxicity data by Dahland Blanck (1996), and an assessment factor for chronic effects of10; whereas Zhang et al. (2008) carried out an assessment bymeans of species sensitivity distribution (SSD) with NOEC valuesfrom saltwater primary producers, leading to a PNECseaw of43.9 ng L�1. If any of these alternative PNECseaw were used in ourstudy, they would result in irgarol being below the risk threshold.Nevertheless, our lower PNECseaw of 0.2 ng L�1 seems to be justifiedwhen experimental studies with phytoplankton communities andmesocosm studies, such as that by Nystrom et al. (2002), havereported NOEC values as low as 8 ng L�1.

3.3. Risk to predators and humans

For both predators and humans, exposure levels lead to a verylow risk for all substances, even with the unrealistic worst-case

Table 4Aquatic ecotoxicity data.

Substance Ecotoxicity to freshwater organisms Ecotoxicity to seawater organisms Assessmentfactore

PNECseaw

(mg L�1)Value (mg L�1) Endpoint Source Value (mg L�1) Endpoint Source

Metronidazole 500 NOEC 3 d in fish Brachydanio rerio Lanzky and Halting-Sørensen, 2000

1060 LC50 4 d in fishCyprinodon variegatus

USEPA (2000) 500 0.025

182 LC50 4 d in crustacean Americamysisbahia (Opossum shrimp)

USEPA (2000) 100 NOEC 3 d in crustaceanAcartia tonsa

Lanzky and Halting-Sørensen, 2000

12.5 EC50 3 d in alga Chlorella sp. Lanzky and Halting-Sørensen, 2000

>1012 EC50 2 d in molluscCrassostrea virginica

USEPA (2000)

Trimethoprim 100 NOEC 3 d in fish Brachyodanio rerio Halling-Sorensen et al. (2000) 1000 0.01692 EC50 2 d in crustacean Daphnia magna Park and Choi (2008)16 EC50 7 d in alga Rhodomonas salina Lutzhoft et al. (1999)

Erythromycin >1000 EC50 3 d in fish Danio rerio Isidori et al. (2005) 4.9 NOEC 2 d in crustaceanPenaeus vannamei

Williams et al., 1992 500 0.00002

0.22 EC50 7 d in crustacean Ceriodaphnia dubia Isidori et al. (2005)0.01 NOEC 3 d in alga

Selenastrum capricornutumEguchi et al. (2004)

Simazine 0.001b

Flumequine 10 NOEC 7 d in fishPimpephales promelas

Robinson et al. (2005) 96.35 EC50 3 d in crustaceanArtemia sp.

Migliore et al. (1997) 500 0.00032

10 NOEC 2 d in crustaceanDaphnia magna

Robinson et al. (2005)

0.159 EC50 7 d in algaMicrocystis aeruginosa

Lutzhoft et al. (1999)

Carbaryl 0.0293 NOEC 1d in fish Ptychocheilus lucius Beyers and Sikoski (1994) 0.0211 LC50 4 d in fish Barbusstigma

Khillare and Wagh (1988) 50 0.00001

0.0005 NOEC 2 d in crustaceanDaphnia magna

Lakota et al. (1981) 0.0015 EC50 2 d in crustaceanPenaeus aztecus

Lowe (1965)

0.1 NOEC 4 d. in algaMicrocystis aeruginosa

Ma et al. (2006) 0.6 EC50 4 d in algaChlorella sp.

Walsh and Alexander (1980)

0.0063 EC50 1.5 d in echinodermPseudechinus magellanicus

Hernandez et al., 1986

1 LOEC 1d in molluscCrassostrea virginica

Butler et al. (1960)

Atrazine 0.0006c

Diuron 0.0002d

Terbutryn 0.82 LC50 4 d in fish Oncorhynchus mykiss Mayer and Ellersieck (1986) 1 EC50 4 d in molluscCrassostrea virginica

Lowe et al. (1970) 1000 2E-06

7.1 EC50 2 d in crustacean Daphnia magna Marchini et al. (1988) 0.022 EC50 1 d in crustaceanArtemia salina

Gaggi et al. (1995)

0.002 EC50 3 d in alga Pseudokirchneriellasubcapitata

Okamura et al. (2000) 0.0031 EC50 4d in algaDunaliella tertiolecta

Gaggi et al. (1995)

Irgarol 0.0061 NOEC subchronic in fishOncorhynchus mykiss

USEPA (2000) 1.58 LC50 4 d in fish Menidiaberyllina

USEPA (2000) 50f 2E-7

5.3 EC50 2d in crustaceanDaphnia magna

USEPA (2000) 0.4 LC50 4 d in crustaceanAmericamysis bahia

USEPA (2000)

0.0001 EC50 5d in diatomNavicula pelliculosa

USEPA (2000) 3.2 EC 50 2 d in molluscCrassostrea virginica

USEPA (2000)

0.0002 EC50 36 d in plantZostera marina

Scarlett et al. (1999)

1E-5 NOEC 4 d in diatomSkeletonema costatum

Zhang et al. (2008)

(continued on next page)

I.Mun oz

etal./

Environmental

Pollution158

(2010)1809–1816

1813

Tab

le4

(con

tin

ued

)

Sub

stan

ceEc

otox

icit

yto

fres

hw

ater

orga

nis

ms

Ecot

oxic

ity

tose

awat

eror

gan

ism

sA

sses

smen

tfa

ctor

ePN

ECse

aw

(mg

L�1)

Val

ue

(mg

L�1)

End

poi

nt

Sou

rce

Val

ue

(mg

L�1)

End

poi

nt

Sou

rce

DPS

49

LC5

04

din

fish

ECO

SAR

a1

00

00

0.0

01

93

0LC

50

2d

ind

aph

nid

ECO

SAR

a

18

.7EC

50

4d

inal

gae

ECO

SAR

a

TCM

TB0

.00

73

LC5

04

din

fish

On

corh

ynch

us

tsh

awyt

sch

aN

ikl

and

Farr

ell

(19

93

)0

.02

03

LC5

04

din

cru

stac

ean

Am

eric

amys

isba

hia

USE

PA(2

00

0)

50

05E

-06

0.0

02

5N

OEC

7d

incr

ust

acea

nC

erio

daph

nia

dubi

aN

awro

cki

etal

.(2

00

5)

60

LC5

04

din

fish

Cyp

rin

odon

vari

egat

us

USE

PA(2

00

0)

0.0

29

LOEC

1.2

5d

inal

gaPs

eudo

kirc

hn

erie

llasu

bcap

itat

a

Fern

and

ez-A

lba

etal

.(2

00

2)

0.0

13

9EC

50

2d

inm

ollu

scM

erce

nar

iam

erce

nar

iaU

SEPA

(20

00

)

aU

SEPA

(20

09

b).

bEC

(20

05

a).

cEC

(20

05

b).

dEC

(20

05

c).

eTa

ble

25

inth

eTG

DR

A,p

art

II(p

.14

9).

fA

ccor

din

gto

the

TGD

RA

(par

tII

,Tab

le2

5),

the

stan

dar

das

sess

men

tfa

ctor

wh

entw

oN

OEC

valu

esar

eav

aila

ble

is5

00

,how

ever

itca

nb

ere

du

ced

to5

0w

hen

thes

eN

OEC

sre

fer

toth

em

ost

sen

siti

vetr

oph

icle

vels

,an

dtw

osh

ort

term

test

son

mar

ine

spec

ies

are

avai

lab

le.

Fig. 1. Risk characterisation for seawater organisms, seawater predators and humans.

I. Munoz et al. / Environmental Pollution 158 (2010) 1809–18161814

approach considered in the exposure assessment. For predators,the highest risk estimate corresponds to DPS, in which exposure is80 times below the adverse-effects level. Although this substancehas a low BCFfish (14 L kg�1), it was the one in the monitoring studywith highest concentrations in seawater (15.5–75.6 ng L�1). Inaddition, the PNECoral used (0.052 mg kgfood

�1 ) is among the lowestfrom the target substances, but this threshold is a rough estimatefrom the oral LD50 in mice. Usually these extrapolations from lethaldoses lead to conservative threshold estimates (Layton et al., 1987),so it is likely that data from chronic feeding studies in mammals/birds would result in a higher PNECoral, entailing a lower RCRpred

than the one determined in our study.With regard to risk to humans, the RCRhuman values are even

lower than those of predators. This is due to the fact that predatorsare assumed to rely on a diet based exclusively on fish, whereas theexposure assessment for humans considers that only part of thediet consists of fish. According to Spanish statistics, finfishconsumption constitutes only 4% by weight of total food intake(excluding beverages).

The low risk predictions for both predators and humans, whichare located at the top of the food chain, are related to the low abilityto bioaccumulate and biomagnify the target pollutants. Accordingto the method suggested in the TGDRA, all the detected substanceshave a BMFfish equal to 1, and with the exception of irgarol, all ofthem have a BCFfish under 100. To date, only those organicsubstances with very high hydrophobicity, such as organochlorinepesticides, polibrominated diphenylethers or polyaromatic hydro-carbons have been shown to pose actual health risks for consumers

I. Munoz et al. / Environmental Pollution 158 (2010) 1809–1816 1815

of farmed fish (Hites et al., 2004; Easton et al., 2002). As a conse-quence, POCIS does not seem to be an appropriate samplingmethod when the focus is on risks at the top of the food chain, sincePOCIS can only be used to analyze compounds with a log Kow up to3–4. Sampling of highly hydrophobic compounds should be carriedout with other passive sampling techniques, such as semi-perme-able membrane devices (SPMD) (Vrana et al., 2005) followed by gaschromatography analysis. SPMD would be useful in analyzing otherchemicals such as vitamin E, butylated hydroxytoluene (BHT) andethoxyquin, which are commonly used in aquaculture feeds butcannot be sampled with POCIS due to their hydrophobicity.

3.4. Potential risk to sediment-dwelling organisms

As has been stated in Section 2.1., potential risks to sediment-dwelling organisms can only be discussed qualitatively, since themonitoring campaign did not include sediment sampling andanalysis, and data from toxicity tests in sediments are scarce.

According to the TGDRA, a log Kow of�3 can be used as a triggercriterion for substances capable of sorbing to sediments. Therefore,from the twelve substances detected in water, only four, namelyerythromycin, terbutryn, irgarol and TCMTB are candidates forsediment toxicity assessment. Exposure and effects in sedimentscan be assessed, at the screening level, using data from the seawatercompartment. This is done by means of the equilibrium partitioningmethod (Di Toro et al., 1991). However, when this method is appliedto data from both exposure and effects, the risk characterisationratios obtained are equivalent to those of seawater (RCRseaw). Thus,if RCRseaw is used as an approximation of the risk to sediment-dwelling organisms, the only substance with a potential hazard isirgarol, which had a RCRseaw of 1.8. Nevertheless, as discussed inSection 3.2, the low PNECseaw of irgarol is related to the high toxicityto primary producers rather than to animals. Since sediments arenot an appropriate environment for primary producers, the toxicitythreshold of irgarol in sediments should be based on the toxicity toanimals, leading to a higher toxicity threshold and thus to a lowerrisk as compared to the seawater compartment.

4. Conclusions

The adverse-effects threshold for seawater organisms wasexceeded by the antifouling irgarol. This substance was found in allthe samples during the monitoring study, with an averageconcentration of 0.36 ng L�1. The seawater ecotoxicity thresholdused for this substance, of 0.2 ng L�1 is determined by the effect onprimary producers, which have been shown in previous studies tobe affected by concentrations as low as 8 ng L�1. The risk to pred-ators and humans through consumption of fish was very low,especially for humans, since the latter are less exposed due to thefact that finfish constitutes only a small part of the diet. The lowmagnitude of the risk estimates for predators and humans is relatedto the low bioaccumulation potential of these substances, due totheir high polarity and low-moderate hydrophobicity. Risks onsediment-dwelling organisms were not assessed quantitatively,although the low hydrophobicity of these substances suggests thattheir ability to accumulate in sediments, and therefore to causeadverse effects, is also low.

Acknowledgements

The authors wish acknowledge to the Spanish Ministry ofEducation and Science for its economical support through projectRef. CTQ2005-09269-C02-0. M.J. Martınez Bueno acknowledges theresearch fellowship from the Junta de Andalucıa (Spain) associatedto project Ref. TEP2329.

References

Alvarez, D.A., Petty, J.D., Huckins, J.N., Jones-Lepp, T.L., Getting, D.T., Goddard, J.P.,Manahan, S.E., 2004. Development of a passive, in situ, integrative sampler forhydrophilic organic contaminants in aquatic environments. Environ. Toxicol.Chem. 23 (7), 1640–1648.

Beyers, D.W., Sikoski, P.J., 1994. Acetylcholinesterase inhibition in federally endan-gered Colorado squawfish exposed to carbaryl and malathion. Environ. Toxicol.Chem. 13 (6), 935–939.

Butler, P.A., Wilson Jr., A.J., Rick, A.J., 1960. Effect of pesticides on Oysters. Proc. Natl.Shellfish Assoc. 51, 23–32.

Ciba Specialty Chemicals Corporation, (2005). Ciba IRGAROL 1051 Material Safetydata Sheet.

Cunningham, V.L., Binks, S.P., Olson, M.J., 2009. Human health risk assessment fromthe presence of human pharmaceuticals in the aquatic environment. Regul.Toxicol. Pharmacol. 53 (1), 39–45.

Dahl, B., Blanck, H., 1996. Toxic effects of the antifouling agent irgarol 1051 on periph-yton communities in coastal water microcosms. Mar. Pollut. Bull. 32 (4), 342–350.

Di Toro, D.M., Zarba, C.S., Hansen, D.J., Berry, W.J., Schwarz, R.C., Cowan, C.E.,Pavlou, S.P., Allen, H.E., Thomas, N.A., Paquin, P.R., 1991. Technical basis ofestablishing sediment quality criteria for non-ionic organic chemicals usingequilibrium partitioning method. Environ. Toxicol. Chem. 10, 1541–1583.

Easton, M.D.L., Luszniak, D., Von der Geest, E., 2002. Preliminary examination ofcontaminated loadings in farmed salmon, wild salmon and commercial salmonfeed. Chemosphere 46, 1053–1074.

EC, 2005a. Common Implementation Strategy for the water framework Directive.Environmental quality standards (EQS) substance data Sheet, priority substanceNo. 29, simazine, CAS-No. 122-34-9. Final version, Brussels.

EC, 2005b. Common Implementation Strategy for the water framework Directive.Environmental quality standards (EQS) substance data Sheet, priority substanceNo. 3, atrazine, CAS-No. 1912-24-9. Final version, Brussels.

EC, 2005c. Common Implementation Strategy for the water framework Directiveenvironmental quality standards (EQS) substance data Sheet, priority substanceNo. 13, diuron, CAS-No. 330-54-1. Final version, Brussels.

Eguchi, K., Nagase, H., Ozawa, M., Endoh, Y.S., Goto, K., Hirata, K., Miyamoto, K.,Yoshimura, H., 2004. Evaluation of antimicrobial agents for veterinary use in theecotoxicity test using microalgae. Chemosphere 57 (11), 1733–1738.

European Commission, 2003. Technical Guidance Document on Risk AssessmentParts I, II, III and IV. European Commission and European Chemicals Bureau,Joint Research Centre, Ispra, Italy.

European Commission, 2004. European Union System for the evaluation ofsubstances 2.0 (EUSES 2.0). Prepared for the European Chemicals Bureau by theNational Institute of Public Health and the Environment (RIVM), Bilthoven, TheNetherlands.

European Parliament, 2000. Directive 2000/60/EC of the European Parliament andof the Council of 23 October 2000 establishing a framework for Communityaction in the field of water policy. Off. J. L 327, 0001–0073. 22.12.00.

European parliament, 2008. Directive 2008/105/EC of the European Parliament andof the Council of 16 December 2008 on environmental quality standards in thefield of water policy, amending and subsequently repealing Council Directives82/176/EEC, 83/513/EEC, 84/156/EEC, 84/491/EEC, 86/280/EEC and amendingDirective 2000/60/EC of the European Parliament and of the Council. Off. J. L348, 0084–0097. 24.12.08.

Falk-Filipsson, A., Hanberg, A., Victorin, K., Warholm, M., Wallen, M., 2007.Assessment factors – applications in health risk assessment of chemicals.Environ. Res. 104, 108–127.

Fernandez-Alba, A.R., Hernando, M.D., Piedra, L., Chisti, Y., 2002. Toxicity evaluationof single and mixed antifouling biocides measured with acute toxicity bioas-says. Anal. Chim. Acta 456 (2), 303–312.

Folke, C., Kautsky, N., Troell, M., 1994. The costs of eutrophication from salmonfarming: implications for policy. J. Environ. Manage. 40 (2), 173–182.

Gaggi, C., Sbrilli, G., El Naby, A.M.H., Bucci, M., Duccini, M., Bacci, E., 1995. Toxicityand hazard ranking of s-triazine herbicides using microtox, two green algalspecies and a marine crustacean. Environ. Toxicol. Chem. 14 (6), 1065–1069.

Graslund, S., Bengtsson, B., 2001. Chemicals and biological products used in south-east Asian shrimp farming, and their potential impact on the environment –a review. Sci. Total Environ. 280, 93–131.

Halling-Sorensen, B., Lutzhoft, H., Andersen, H., Ingerslev, F., 2000. Environmentalrisk assessment of antibiotics: comparison of mecillinam, trimethoprim andciprofloxacin. J. Antimicrob. Chemother. 46, 53–58.

Heggberget, T.G., Johnsen, B.O., Hindar, K., Jonsson, B., Hansen, L.P., Hvidsten, N.A.,Jensen, A.J., 1993. Interactions between wild and cultured Atlantic salmon:a review of the Norwegian experience. Fish. Res. 18 (1–2), 123–146.

Hernandez, D.A., Lombardo, R.J., Ferrari, L., Tortorelli, M.C., 1986. Toxicidad Del Etil-Paration y Carbaril Sobre Estadios Tempranos Del Desarrollo Del Erizo De Mar.(Toxicity of ethil-parathion and carbaryl on early stages of the development ofsea urchin). ce: Arch. Biol. Med. Exp. 19 (2), R212.

Hites, R.A., Foran, J.A., Carpenter, D.O., Hamilton, M.C., Knuth, B.A., Schwager, S.J.,2004. Global assessment of organic contaminants in farmed salmon. Science303, 226–229.

Huntington, T.C., Roberts, H., Cousins, N., Pitta, V., Marchesi, N., Sanmamed, A.,Hunter-Rowe, T., Fernandes, T.F., Tett, P., McCue J., Brockie, N., 2006. SomeAspects of the environmental impact of aquaculture in sensitive areas. Report tothe DG Fish and Maritime Affairs of the European Commission.

I. Munoz et al. / Environmental Pollution 158 (2010) 1809–18161816

Isidori, M., Lavorgna, M., Nardelli, A., Pascarella, L., Parrella, A., 2005. Toxic andgenotoxic evaluation of six antibiotics on non-target organisms. Sci. TotalEnviron. 346 (1–3), 87–98.

JECFA-Joint FAO/WHO Expert Committee on Food Additives, 2004. WHO FoodAdditives Series: 53, Flumequine (addendum). http://www.inchem.org/documents/jecfa/jecmono/v53je06.htm. Accessed 21.04.09.

Kanazawa, J., 1980. Prediction of biological concentration potential of pesticides inaquatic organisms. Rev. Plant Prot. Res. 13, 27–36.

Khillare, Y.K., Wagh, S.B.,1988. Acute toxicity of pesticides in the freshwater fish Barbusstigma: histopathology of the stomach. Uttar Pradesh J. Zool. 8 (2), 176–179.

Konstantinou, I.K., Albanis, T.A., 2004. Worldwide occurrence and effects of anti-fouling paint booster biocides in the aquatic environment: a review. Environ.Int. 30 (2), 235–248.

Lakota, S., Raszka, A., Kupczak, I., 1981. Toxic Effect of Cartap, Carbaryl, and Propoxuron Some Aquatic Organisms. Acta Hydrobiol. 23 (2), 183–190.

Lanzky, P.F., Halting-Sørensen, B., 2000. The toxic effect of the antibiotic metroni-dazole on aquatic organisms. Chemosphere 35 (11), 2553–2561.

Layton, D.W., Mallon, B.J., Rosenblatt, D.H., Small, M.J., 1987. Deriving allowabledaily intakes for systemic toxicants lacking chronic toxicity data. Regul. Toxicol.Pharm. 7, 96–112.

Lowe, J.I., 1965. Results of toxicity tests with Fishes and Macroinvertebrates. Unpub-lished Data, Data Sheets available from U.S. EPA Res. Lab., Gulf Breeze, FL :81 p.

Lowe, J.I., Wilson, P.D., Davison, R.B., 1970. Laboratory Bioassays, 335. U.S. Fish Wildl.Serv., Circ, Washington, DC, pp. 20–23.

Loya, Y., Lubinevsky, H., Rosenfeld, M., Kramarsky-Winter, E., 2004. Nutrientenrichment caused by in situ fish farms at Eilat, Red Sea is detrimental to coralreproduction. Mar. Pollut. Bull. 49 (4), 344–353.

Lutzhoft, H.C.H., Halling-Sorensen, B., Jorgensen, S.E., 1999. Algal toxicity of anti-bacterial agents applied in Danish fish farming. Arch. Environ. Contamin. Tox-icol. 36, 1–6.

Ma, J., Lu, N., Qin, W., Xu, R., Wang, Y., Chen, X., 2006. Differential responses of eightcyanobacterial and green algal species, to carbamate insecticides. Ecotoxicol.Environ. Saf. 3 (2), 268–274.

Marchini, S., Passerini, L., Cesareo, D., Tosato, M.L., 1988. Herbicidal Triazines: AcuteToxicity on Daphnia, Fish, and Plants and Analysis of its Relationships withStructural Factors. Ecotoxicol. Environ. Saf 16 (2), 148–157.

Martınez Bueno, M.J., Hernando, M.D., Aguera, A., Fernandez-Alba, A.R., 2009.Application of passive sampling devices for screening of micro-pollutants inmarine aquaculture using LC–MS/MS. Talanta 77, 1518–1527.

Mayer, F.L.Jr., Ellersieck, 1986. Manual of Acute toxicity: interpretation and data Basefor 410 chemicals and 66 species of freshwater Animals. Resour. Publ. No.160,U.S. Dep. Interior, Fish Wildl. Serv., Washington, DC.

Meylan, W.M., Howard, P.H., Boethling, R.S., Aronson, D., Printup, H., Gouchie, S., 1999.Improved method for estimating bioconcentration/bioaccumulation factor fromoctanol/water partition coefficient. Environ. Toxicol. Chem. 18 (4), 664–672.

Migliore, L., Civitareale, C., Brambilla, G., Dojmi di Delupis, G., 1997. Toxicity of severalimportant agricultural antibiotics to Artemia. Water Res. 31 (7), 1801–1806.

Ministerio de Agricultura, 2006. Pesca y Alimentacion. La alimentacion en Espana,Madrid.

Morley, N.J., Leung, K.M.Y., Morritt, D., Crane, M., 2003. Toxicity of anti-foulingbiocides to Parorchis acanthus (Digenea: Philophthalmidae) cercarial encyst-ment. Dis. Aquat. Org. 54, 55–60.

Munoz, I., Gomez, M.J., Molina-Dıaz, A., Huijbregts, M.A.J., Fernandez-Alba, A.R.,Garcıa-Calvo, E., 2008. Ranking potential impacts of priority and emergingpollutants in urban wastewater through life cycle impact assessment. Chemo-sphere 74 (1), 37–44.

Nawrocki, S.T., Drake, K.D., Watson, C.F., Foster, G.D., Maier, K.J., 2005. Comparativeaquatic toxicity evaluation of 2-(thiocyanomethylthio)benzothiazole andselected degradation products using ceriodaphnia dubia. Arch. Environ. Con-tam. Toxicol. 48 (3), 344–350.

Naylor, R.L., Goldburg, R.J., Primavera, J.H., Kautsky, N., Beveridge, M.C.M., Clay, J.,Folke, C., Lubchenco, J., Mooney, H., Troell, M., 2000. Effect of aquaculture onworld fish supplies. Nature 405, 1017–1024.

Nierentz, J., 2007. Overview of production and trade – the role of aquaculture fishsupply. In: Arthur, R, Nierentz, J. Global Trade Conference on Aquaculture.Proceedings of the Conference Held in Qingdao, China, 29–31 May, 2007. FAOFisheries Proceedings n�9, Rome.

Nikl, D.L., Farrell, A.P.,1993. Reduced swimming performance and gill structural changesin juvenile salmonids exposed to 2-(thiocyanomethylthio)benzothiazole. Aquat.Toxicol. 27 (3/4), 245–264.

Nystrom, B., Becker-Van Slooten, K., Berard, A., Grandjean, D., Druart, J.C.,Leboulanger, C., 2002. Toxic effects of Irgarol 1051 on phytoplankton andmacrophytes in Lake. Geneva 36 (8), 2020–2028.

Okamura, H., Aoyama, I., Liu, D., Maguire, R.J., Pacepavicius, G.J., Lau, Y.L., 2000. Fateand Ecotoxicity of the new Antifouling Compound Irgarol 1051 in the AquaticEnvironment. Water Res. 34 (14), 3523–3530.

Paez-Osuna, F., 2001. The environmental impact of shrimp aquaculture: causes,effects, and mitigating alternatives. Environ. Manage. 28 (1), 131–140.

Park, S., Choi, K., 2008. Hazard assessment of commonly used agricultural antibi-otics on aquatic ecosystems. Ecotoxicology 17 (6), 526–538.

Piedra, L., Tejedor, A., Hernando, M.D., Aguera, A., Barcelo, D., Fernandez-Alba, A.,2000. Screening of antifouling pesticides in sea water samples at low ppt levelsby GC–MS and LC–MS. Chromatographia 52, 631–638.

Pouliquen, H., Delepee, R., Larhantec-Verdier, M., Morvan, M., Le Bris, H., 2007.Comparative hydrolysis and photolysis of four antibacterial agents (oxytetra-cycline oxolinic acid, flumequine and florfenicol) in deionised water, freshwaterand seawater under abiotic conditions. Aquaculture 262, 23–28.

PPDB, (2009). The Pesticide Properties DataBase (PPDB) developed by the Agri-culture & Environment Research Unit (AERU) at the University of Hertford-shire, from the database that originally accompanied the EMA(Environmental Management for Agriculture) software (also developed byAERU), with additional input from the EU-funded FOOTPRINT project (FP6-SSP-022704).

Read, P., Fernandes, T., 2003. Management of environmental impacts of marineaquaculture in Europe. Aquaculture 226, 139–163.

Robinson, A.A., Belden, J.B., Lydy, M.J., 2005. Toxicity of fluoroquinolone antibioticsto aquatic organisms. Environ. Toxicol. Chem. 24 (2), 423–430.

Sakkas, V.A., Konstantinou, I.K., Lambropoulou, D.A., Albanis, T.A., 2002. Survey forthe occurrence of antifouling paint booster biocides in the aquatic environmentof Greece. Environ. Sci. Pollut. Res. 9 (5), 327–332.

Scarlett, A., Donkin, P., Fileman, T.W., Evans, S.V., Donkin, M.E., 1999. Risk posed bythe antifouling agent irgarol 1051 to the seagrass, Zostera marina. Aquat. Tox-icol. 45 (2/3), 159–170.

Schwab, B.W., Hayes, E.P., Fiori, J.M., Mastrocco, F.J., Roden, N.M., Cragin, D.,Meyerhoff, R.D., D’Aco, V.J., Anderson, P.D., 2005. Human pharmaceuticals in USsurface waters: a human health risk assessment. Regul. Toxicol. Pharmacol. 42(3), 296–312.

Siracuse Research Corporation, 2009. Interactive PhysProp Database Demo. http://www.srcinc.com/what-we-do/databaseforms.aspx?id¼386. Accessed 20.04.09.

Thomas, K.V., Fileman, T.W., Readman, J.W., Waldock, M.J., 2001. Antifouling paintbooster biocides in the UK coastal environment and potential risks of biologicaleffects. Mar. Pollut. Bull. 42 (8), 677–688.

U.S. National Library of Medicine, 2009. ChemIDplus Advanced. http://chem.sis.nlm.nih.gov/ChemIDplus/. Accessed in March 2009.

USEPA, 2000. Pesticide Ecotoxicity Database (Formerly: Environmental EffectsDatabase (EEDB)). Office of Pesticide Programs, Environmental Fate and EffectsDivision, Washington, DC.

USEPA, 2006. 2-(Thiocyanomethylthio) benzothiazole (TCMTB) Preliminary RiskAssessment for the Reregistration Eligibility Decision (RED) Document. Wash-ington, DC.

USEPA, 2009a. Ecotox Release 4.0. http://cfpub.epa.gov/ecotox/. Accessed in March2009.

USEPA, 2009b. ECOSAR (Ecological Struct. Activity Relationships) v. 1.00. OPPT –Risk Assessment Division.

USEPA, 2009c. Integrated Risk Information System. http://www.epa.gov/IRIS/.Accessed in March 2009.

Vrana, B., Mills, G.A., Allan, I.J., Dominiak, E., Svensson, K., Knutsson, J., Morrison, G.,Greenwood, R., 2005. Passive sampling techniques for monitoring pollutants inwater. Trends in Analytical Chemistry 24 (10), 845–868.

Walsh, G.E., Alexander, S.V., 1980. A marine algal bioassay method: results withpesticides and industrial wastes. Water Air Soil Pollut. 13 (1), 45–55.

Williams, R.R., Bell, T.A., Lightner, D.V., 1992. Shrimp antimicrobial testing. II.Toxicity testing and safety determination for twelve antimicrobials withpenaeid shrimp Larvae. J. Aquat. Anim. Health 4 (4), 262–270.

Youngson, A.F., Dosdat, A., Saroglia, M., Jordan, W.C., 2001. Genetic interactionsbetween marine finfish species in European aquaculture and wild conspecifics.J. Appl. Ichthyol. 17 (4), 153–162.

Zhang, A.Q., Leung, K.M.Y., Kwok, K.W.H., Bao, V.W.W., Lam, M.H.W., 2008. Toxicitiesof antifouling biocide Irgarol 1051 and its major degraded product to marineprimary producers. Mar. Pollut. Bull. 57, 575–586.