Inhibition of coral photosynthesis by the antifouling herbicide Irgarol 1051

International regulation of organotin compounds for use in antifouling paints has led to the development and increased use of replacement compounds, notably the s-triazine herbicide Irgarol 1051. Little is known about the distribution of Irgarol 1051 in tropical waters. Nor has the potential impact of this triazine upon photosynthesis of endosymbiotic microalgae (zooxanthellae) in corals been assessed. In this study Irgarol 1051 was detected in marinas, harbours and coastal waters of the Florida Keys, Bermuda and St. Croix, with concentrations ranging between 3 and 294 ng 1(-1). 14C incubation experiments with isolated zooxanthellae from the common inshore coral Madracis mirabilis showed no incorporation of H14CO3- from the sea water medium after 4-8 h exposure to Irgarol 1051 concentrations as low as 63 ng 1(-1). Reduction in net photosynthesis of intact corals was found at concentrations of l00 ng 1(-1) with little or no photosynthesis at concentrations exceeding 1000 ng 1(-1) after 2-8 h exposure at all irradiances. The data suggest Irgarol 1051 to be both prevalent in tropical marine ecosystems and a potent inhibitor of coral photosynthesis at environmentally relevant concentrations.     

Antifouling herbicides in the coastal waters of western Japan

Residue analyses of some antifouling herbicides (Diuron, Irgarol 1051 and the latter's degradation product M1, which is also known as GS26575), were conducted in waters collected along the coast of western Japan. In total, 142 water samples were collected from fishery harbours (99 sites), marinas (27 sites), and small ports (16 sites) around the Seto Inland Sea, the Kii Peninsula, and Lake Biwa, in August 1999. A urea-based herbicide, Diuron, was positively identified for the first time in Japanese aquatic environments. Diuron was detected in 121 samples (86%) up to a highest concentration of 3.05 microg/l, and was found in 86% of samples from fishery harbours, 89% from marinas, and 75% from ports. Four freshwater samples out of 11 collected at Lake Biwa contained Diuron. Neither Irgarol 1051 nor M1 was found in the lake waters, but both were found in many coastal waters. Irgarol 1051 was found in 84 samples (60%) at a highest concentration of 0.262 microg/l. The concentrations detected were of similar magnitude to those in our previous surveys, taken in 1997 and 1998. M1 was found in 40 samples (28%) up to a highest concentration of 0.080 microg/l. The concentrations detected were generally lower than those found in our previous surveys. The detection frequency among fishery harbours, marinas, and ports was 57-70% for Irgarol 1051 and 25-30% for M1. Ninety-five per cent of the coastal waters in which M1 was detected also contained Irgarol 1051, and 93% of the samples in which Irgarol 1051 was detected also contained Diuron. These results clearly suggest that commercial ship-bottom paints containing both Diuron and Irgarol 1051 are used extensively in the survey area.     

Contamination of the coastal waters of Bermuda by organotins and the triazine herbicide Irgarol 1051.

A study of the distribution of the 'booster' biocide 2-methylthio-4-tert-butylamino-6-cyclopropyl amino-s-triazine (Irgarol 1051) was carried out in the coastal waters of Bermuda. Irgarol 1051 concentrations (as determined by GC/MS) up to 590 ng l-1 have been measured within Hamilton Harbour. The data presented herein unequivocally demonstrate contamination of the coastal system of Bermuda by Irgarol 1051. Concurrently, TBT concentrations were measured and results indicate that levels are falling through legislated changes in antifouling treatments, from 220 ng l-1 in 1990 to < 20 ng l-1 (as Sn) by 1995, in the open water area of Hamilton Harbour. Concentrations of TBT immediately offshore from a boatyard were found to be > 600 ng l-1 (Sn), indicating continuing release due to painting operations and sediments in the area.     

Occurrence and transport of Irgarol 1051 and its major metabolite in coastal waters from South Florida

Irgarol 1051, a boosting antifouling agent often used to supplement copper based paints was found in surface waters from South Florida at stations collected from the Miami River, Biscayne Bay and selected areas of the Florida Keys. Concentrations of the herbicide ranged from below the method detection limit (1 ng/L) to as high as 182 ng/L in a canal system in Key Largo. The herbicide was present at 93% of the stations and often found in conjunction with its descyclopropyl metabolite (M1) previously reported to be the major degradation product of Irgarol under natural environmental conditions. The 90th percentile concentration calculated for all South Florida samples was 57.6 ng/L. Based on available data on the toxicity of Irgarol to algae and coral, only two stations (approximately 3%) ranked above the LC50 of 136 ng/L reported for the marine algae Naviculla pelliculosa and above the 100 ng/L level reported to reversibly inhibit photosynthesis of intact corals. However, a basic dissipation model for Irgarol using the Key Largo Harbor station as a point source indicated that concentrations of the herbicide decreased rapidly and concentrations below the MDL are observed within 2000 m of the source. No major coral based benthic habitats are documented for all the stations surveyed at distances that Irgarol may pose a substantial risk. However, other types of submerged vegetation like seagrasses are common around the marinas and the effects of Irgarol to such endpoints should be investigated further.     

Photosystem II herbicide pollution in Hong Kong and its potential photosynthetic effects on corals

Photosystem II (PSII) herbicides have been shown to affect the photosynthesis of corals at low, environmentally relevant concentrations. The recent detection of the PSII herbicide Irgarol-1051 in coastal waters of Hong Kong at concentrations above the EC(50) for reduction of photosynthesis of corals prompted further investigation into the extent of PSII herbicide pollution in coral reefs of Hong Kong. Snap-shot and passive samples were taken from coral reef sites and evaluated via HPLC/MS-MS and a novel bioanalytical technique. Low concentrations (less than 10 ng L(-1)) of diuron and atrazine were found at all study sites. Extracts from these samples concentrated by a factor of 10 were found to reduce the photosynthetic yield of zooxanthellae. It appears unlikely that herbicide pollution is a key issue in isolation but may act synergistically with other stressors to reduce the viability of Hong Kong's coral reefs. The study has also demonstrated the feasibility of combining sample extraction techniques with a coral specific bioanalytical technique for a sensitive assessment of risks associated with herbicide exposure in corals.     

Photosystem II herbicide pollution in Hong Kong and its potential photosynthetic effects on corals

Photosystem II (PSII) herbicides have been shown to affect the photosynthesis of corals at low, environmentally relevant concentrations. The recent detection of the PSII herbicide Irgarol-1051 in coastal waters of Hong Kong at concentrations above the EC₅₀ for reduction of photosynthesis of corals prompted further investigation into the extent of PSII herbicide pollution in coral reefs of Hong Kong. Snap-shot and passive samples were taken from coral reef sites and evaluated via HPLC/MS–MS and a novel bioanalytical technique. Low concentrations (less than 10 ng L⁻¹) of diuron and atrazine were found at all study sites. Extracts from these samples concentrated by a factor of 10 were found to reduce the photosynthetic yield of zooxanthellae. It appears unlikely that herbicide pollution is a key issue in isolation but may act synergistically with other stressors to reduce the viability of Hong Kong’s coral reefs. The study has also demonstrated the feasibility of combining sample extraction techniques with a coral specific bioanalytical technique for a sensitive assessment of risks associated with herbicide exposure in corals.     

Antifouling paint booster biocides in the UK coastal environment and potential risks of biological effects

In the yachting sector of the UK antifouling market, organic biocides are commonly added to antifouling preparations to boost performance. Few data presently exist for concentrations of these compounds in UK waters. In this study the concentrations of tributyltin (TBT) and eight booster biocides were measured before and during the 1998 yachting season. The Crouch Estuary, Essex, Sutton Harbour, Plymouth and Southampton Water were chosen as representative study sites for comparison with previous surveys of TBT concentrations. Diuron and Irgarol 1051 were the only organic booster biocides found at concentrations above the limits of detection. Diuron was measured at the highest concentrations, whilst detectable concentrations of both Irgarol 1051 and diuron were determined in areas of high yachting activity (e.g. mooring areas and marinas). Maximum measured values were 1,421 and 6,740 ng/l, respectively. Lower concentrations of both compounds were found in open estuarine areas, although non-antifouling contributions of diuron may contribute to the overall inputs to estuarine systems. TBT was found to be below or near the environmental quality standard (EQS) of 2 ng/l for all samples collected from estuarine areas frequented by pleasure craft alone, but with much higher concentrations measured in some marinas, harbours and in areas frequented by large commercial vessels. Using the limited published environmental fate and toxicity data available for antifouling booster biocides, a comparative assessment to evaluate the risk posed by these compounds to the aquatic environment is described. TBT still exceeds risk quotients by the greatest margins, but widespread effects due to Irgarol 1051 and less so diuron cannot be ruled out (particularly if use patterns change) and more information is required to provide a robust risk assessment.     

Assessing the effects of Irgarol 1051 on marine phytoplankton populations in Key Largo Harbor, Florida

The antifouling boosting agent Irgarol 1051 is a strong inhibitor of the photosystem II (PSII) with high efficiency/toxicity towards algae. However, because some phytoplankton species are more sensitive to Irgarol than others, its persistent release into the environment could result in adverse changes in the phytoplankton community structure at heavily impacted sites such as marinas. Continuous monitoring in the Florida Keys showed Irgarol concentrations of up to 635 ngL(-1) in the canal system leading to Key Largo Harbor Marina (KLH) with a sharp decrease in concentration at stations offshore from the mouth of the canal. Preliminary phytoplankton community assessments from surface water samples collected in KLH between February and August 2004 showed changes in several phytoplankton species in concordance with the increase of the herbicide concentrations. Typical responses include an increase in the abundance of eukaryotes and Cryptomonas sp. as Irgarol concentrations increase.     

Occurrence of Irgarol 1051 and its major metabolite in Maryland waters of Chesapeake Bay

Irgarol and its major metabolite (GS26575) were measured in Maryland waters of Chesapeake Bay: (1) in and near 10 marinas, a mainstem Bay site and two Severn River locations during a general survey in July and December of 2002; (2) at various sites in the Port Annapolis Marina and the Severn River area during March of 2002 before the boating season began; and (3) during July (peak boating season) in the same Port Annapolis Marina and Severn River sites area during both an ebb and flood tide. Irgarol concentrations ranged from 1.82 ng/l at the mid-Bay site to 585 ng/l in Port Annapolis marina during the July and December general survey. An Irgarol 90th centile of 239 ng/l was reported for the 10 marina sites, two Severn River sites and one mainstem site sampled during the general survey conducted in July and December. Temporal analysis of all pooled data showed that 90th centiles were over seven times higher in July when compared to December. A comparison of Irgarol concentrations at 12 sites in the Port Annapolis marina and Severn River area during both an ebb and flood tide in July showed no consistent trend with tidal cycle by site although significant reductions in concentrations were reported with distance from the three Port Annapolis marina sites. Ecological risk from Irgarol exposure was judged to be low for most Chesapeake Bay sites sampled. Possible exceptions were Port Annapolis marina, Severn River sites in close proximity to this marina and Chesapeake Harbor marina where Irgarol concentrations exceeded a conservative effects threshold during the peak boating season in July. Ecological risk from GS26575 exposure was low for all sites.     

The impact of legislation on the usage and environmental concentrations of Irgarol 1051 in UK coastal waters

In 2001, legislative measures were introduced in the UK to restrict usage of antifouling agents in small (<25 m) vessel paints to dichlofluanid, zinc pyrithione and zineb. This removed the previously popular booster biocides diuron and Irgarol 1051 from the market. To investigate the impact of this legislation, water samples were taken from locations where previous biocide levels were well documented. Results from analyses demonstrate a clear reduction in water concentrations of Irgarol 1051 (between 10% and 55% of that found during pre-restriction studies), indicating that legislation appears to have been effective. Although other booster biocides were screened for (chlorothalonil, dichlofluanid and Sea-Nine 211), they were below the limits of detection (<1 ng/l) in all samples. A survey of chandlers and discussions with legislative authorities supports these results and concurs the removal of Irgarol 1051 based paints from the market using simple regulations at a manufacturer level with little regulation at a retailer level.     

The relationship of Irgarol and its major metabolite to resident phytoplankton communities in a Maryland marina, river and reference area

The objectives of this study were to: (1) measure water column concentrations of Irgarol 1051 and its major metabolite GS26575 annually (2004-2006) during mid-June and mid-August at 14 sites in a study area comprised of three sub-regions chosen to reflect a gradient in Irgarol exposure (Port Annapolis marina, Severn River and Severn River reference area); (2) use a probabilistic approach to determine ecological risk of Irgarol and its major metabolite in the study area by comparing the distribution of exposure data with toxicity-effects endpoints; and (3) measure both functional and structural resident phytoplankton parameters concurrently with Irgarol and metabolite concentrations to assess relationships and determine ecological risk at six selected sites in the three study areas described above. The three-year summer mean Irgarol concentrations by site clearly showed a gradient in concentrations with greater values in Back Creek (400-500 ng/L range), lower values in the Severn River sites near the confluence with Back Creek (generally values less than 100 ng/L) and still lower values (<10 ng/L) at the Severn River reference sites at the confluence with Chesapeake Bay. A similar spatial trend, but with much lower concentrations, was also reported for GS26575. The probability of exceeding the Irgarol plant 10th centile of 193 ng/L and the microcosm NOEC (323 ng/L) suggested high ecological risk from Irgarol exposure at Port Annapolis marina sites but much lower risk at the other sites. There were no statistically significant differences among the three site types (marina, river and reference) with all years combined or among years within a site type for the following functional and structural phytoplankton endpoints: algal biomass, gross photosynthesis, biomass normalized photosynthesis, chlorophyll a, chlorophyll a normalized photosynthesis and taxa richness. Therefore, based on the above results, Irgarol adverse effects predicted from the plant 10th centile and the microcosm NOEC in the high Irgarol exposure area (Back Creek/Port Annapolis marina) were not confirmed with the actual field data for the receptor species (phytoplankton). These results also highlight the importance of unconfined field studies with a chemical gradient in providing valuable information regarding the responses of resident phytoplankton to herbicides.     

Tributyltin along the coasts of Corsica (Western Mediterranean): a persistent problem.

Despite optimistic forecasts by various scientists after regulatory measures were taken in the 1980s, coastal tributyltin (TBT) contamination is still a major problem. The present study concerning Corsica (Western Mediterranean) shows that contamination is not limited to harbour areas, but extends along the coast, involving protected nature reserves. The concentrations measured in harbours, which can reach 200 ng TBT l(-1), tend to incriminate both pleasure craft and ferries providing regular service between the island and the continent. Contamination as high as 7 ng TBT l(-1) has been measured in waters of the Scandola nature reserve, which is quite excessive given the no effect concentrations (NOEC) for marine fauna are around 1-2 ng TBT l(-1). The inadequacy of current regulations and their application are a major factor in this situation.     

Antifouling biocides in water and sediments from California marinas

Irgarol 1051 is a common antifouling biocide and is highly toxic to non-target plant species at low ng/L concentrations. We measured up to 254 ng/L Irgarol in water and up to 9 ng/g dry weight Irgarol in sediments from Southern California recreational marinas. Irgarol’s metabolite, M1, concentrations were up to 62 ng/L in water and 5 ng/g dry weight in sediments. Another antifouling biocide, diuron, reached up to 68 ng/L in water and 4 ng/g dry weight in sediments. The maximum Irgarol concentrations in water were greater than the Irgarol concentration recommended as the plant toxicity benchmark (136 ng/L), suggesting that Irgarol concentrations may be high enough to cause changes in phytoplankton communities in the sampled marinas. Irgarol concentrations measured in sediments were greater than calculated Environmental Risk Limits (ERLs) for Irgarol in sediments (1.4 ng/g). Antifouling pesticide accumulation in sediments may present a potential undetermined risk for benthic organisms.     

Assessment of TBT and organic booster biocide contamination in seawater from coastal areas of South Korea

Seawater samples from major enclosed bays, fishing ports, and harbors of Korea were analyzed to determine levels of tributyltin (TBT) and booster biocides, which are antifouling agents used as alternatives to TBT. TBT levels were in the range of not detected (nd) to 23.9 ng Sn/L. Diuron and Irgarol 1051, at concentration ranges of 35–1360 ng/L and nd to 14 ng/L, respectively, were the most common alternative biocides present in seawater, with the highest concentrations detected in fishing ports. Hot spots were identified where TBT levels exceeded environmental quality targets even 6 years after a total ban on its use in Korea. Diuron exceeded the UK environmental quality standard (EQS) value in 73% of the fishing port samples, 64% of the major bays, and 42% of the harbors. Irgarol 1051 levels were marginally below the Dutch and UK EQS values at all sites.     

Toxicities of antifouling biocide Irgarol 1051 and its major degraded product to marine primary producers

Irgarol 1051 (2-methythiol-4-tert-butylamino-6-cyclopropylamino-s-triazine) is an algaecide commonly used in antifouling paints. It undergoes photodegradation which yields M1 (2-methylthio-4-tert-butylamino-6-amino-s-triazine) as its major and most stable degradant. Elevated levels of both Irgarol and M1 have been detected in coastal waters worldwide; however, ecotoxicity effects of M1 to various marine autotrophs such as cyanobacteria are still largely unknown. This study firstly examined and compared the 96 h toxicities of Irgarol and M1 to the cyanobacterium Chroococcus minor and two marine diatom species, Skeletonema costatum and Thalassiosira pseudonana. Our results suggested that Irgarol was consistently more toxic to all of the three species than M1 (96 h EC50 values: C. minor, 7.71 microug L(-1) Irgarol vs. > 200 microg L(-1) M1; S. costatum, 0.29 microg L(-1) Irgarol vs. 11.32 microg L(-1)M1; and T. pseudonana, 0.41 microg L(-1) Irgarol vs. 16.50 microg L(-1)M1). Secondly, we conducted a meta-analysis of currently available data on toxicities of Irgarol and M1 to both freshwater and marine primary producers based on species sensitivity distributions (SSDs). Interestingly, freshwater autotrophs are more sensitive to Irgarol than their marine counterparts. For marine autotrophs, microalgae are generally more sensitive to Irgarol than macroalgae and cyanobacteria. With very limited available data on M1 (i.e. five species), M1 might be less toxic than Irgarol; nonetheless this finding warrants further confirmation with additional data on other autotrophic species.     

Seasonal variability in the concentrations of Irgarol 1051 in Brighton Marina,UK; including the impact of dredging

Variations in Irgarol 1051 concentrations in the UK's largest marina at Brighton were determined regularly over a period of one year. Aqueous concentrations ranged from <1 to 960 ngl(-1) with highest mean concentrations generally associated with berths for larger vessels and with the main channels. Temporally, highest concentrations were recorded in November through to January and were probably associated with maintenance of vessels in an adjacent boatyard. Elevated levels were also encountered at the beginning of the season, coinciding with the introduction of newly antifouled vessels. Increased concentrations also followed dredging, possibly through re-mobilisation of Irgarol 1051. No correlations were found between dissolved Irgarol 1051 concentrations and pH, temperature or salinity. With the exception of sporadically high concentrations recorded for water samples (probably taken in close proximity to recently antifouled vessels), concentrations rarely exceeded the no observed effect concentration for marine periphyton of 63 ngl(-1). Concentrations of Irgarol 1051 in sediments sampled from the marina ranged from <1 to 77 ngg(-1). Apparent distribution coefficients (K(d)) calculated from sedimentary and aqueous samples (collected simultaneously) are generally within the range of K(d)'s reported from laboratory experiments.     

A survey of antifoulants in sediments from Ports and Marinas along the French Mediterranean coast

Due to deleterious effects on non-target organisms, the use of organotin compounds on boat hulls of small vessels (<25 m) has been widely prohibited. The International Maritime Organisation (IMO) resolved that the complete prohibition on organotin compounds acting as biocides in antifouling systems should commence in 2008. As a result of restrictions on the use of organotin based paints, other antifouling formulations containing organic biocides have been utilised. This survey was conducted to assess the contamination of replacement biocides in the marine environment following the ban of TBT-based paints. Surface sediments samples were collected in the major ports and marinas along the France Mediterranean coastline (Cote d’Azur) and analysed for organotin compounds, Irgarol 1051, Sea-nine 211^TM, Chlorothalonil, Dichlofluanid and Folpet. Every port and marina exhibited high levels of organotin compounds, with concentrations in sediments ranging from 37 ng Sn g⁻¹dry wt in Menton Garavan to over 4000 ng Sn g⁻¹dry wt close to the ship chandler within the port of Villefranche-sur-Mer. TBT degradation indexes suggested that fresh inputs are still made. Among the other antifoulants monitored, only Irgarol 1051 exhibited measurable concentrations in almost every port, with concentrations ranging from 40 ng g⁻¹dry wt (Cannes) to almost 700 ng g⁻¹dry wt (Villefranche-sur-Mer, ship chandler).     

Occurrence of IRGAROL 1051 in coastal waters from Biscayne Bay,Florida, USA

Surface water samples from marinas, commercial ports and open bay areas collected from Biscayne Bay and the Miami River, Florida, USA, were analyzed for the occurrence of IRGAROL 1051 by GC/MS. The anifouling boosting herbicide was found in 80% (46/57) of the samples collected between March 1999 and September 2000. Concentrations within the bay range between non-detected (<1 ppt) and 61 ppt (ng/L) and were generally low compared with levels reported in European or Japanese waters. Aside from the elevated concentrations observed along the Miami River South Fork (61 ppt), the highest concentrations observed in the bay corresponded to marinas with high density of pleasure craft and restricted water circulation. In contrast, occurrence of IRGAROL 1051 along the commercial port or the cruise line terminal was generally lower (<1-2.2 ppt). Concentrations around Coconut Grove Marina were consistently higher (5-12 ppt) than the rest of the bay waters during the whole period of time surveyed.     

Extreme irgarol tolerance in an Ulva lactuca L. population on the Swedish west coast

The herbicide irgarol 1051 is commonly used on ship hulls to prevent growth of algae, but as a component of self-eroding paints it can also spread in the surrounding waters and affect non-target organisms. The effect of irgarol on settlement and growth of zoospores from the marine macro algae Ulva lactuca from the Gullmar fjord on the Swedish west coast was investigated in the present study. The zoospores were allowed to settle and grow in the presence of irgarol, but neither settlement – nor growth inhibition was observed at concentrations of up to 2000 nmol l⁻¹. This is between 10 and 100 times higher than effect concentrations reported earlier for algae. Irgarol also induced the greening effect (4-fold increase in chlorophyll a content) in the settled zoospore/germling population, typical for photosystem II inhibitors like irgarol. This study support previous findings that irgarol constitutes a selection pressure in the marine environment.     

Concentrations of methyl- tert-butyl ether (MTBE) in inputs and receiving waters of Southern California.

The occurrence and concentration of the fuel additive methyl-tert-butyl ether (MTBE) were measured in dry weather runoff, municipal wastewater and industrial effluents, and coastal receiving waters in southern California. Combined, refineries and sewage treatment plants release approximately 214 kg day(-1) of MTBE into the marine environment, with Santa Monica Bay receiving most (98%) of this discharge. Dry weather urban runoff was analysed for samples collected from 25 streams and rivers, and accounted for less than 0.5% of the mass of MTBE discharged to coastal waters. Receiving water samples were collected from 23 stations in Santa Monica Bay, Los Angeles Harbour and Mission Bay or San Diego Bay. MTBE was detected at low concentrations near effluent discharges, however there was no evidence of baywide MTBE contamination related to these outfalls. Marinas and areas used intensively for recreational boating had the highest average MTBE concentration (8.8 microg l(-1)). Surface water contamination was most widespread in San Diego Bay and Mission Bay, areas with no refinery or sewage treatment plant inputs.