- Email: [email protected]
Use of semipermeable membrane devices to investigate the impacts of DDT (Dichlorodiphenyltrichloroethane) in the Holland Marsh environs of the Lake Simcoe watershed (Ontario, Canada)
Journal of Great Lakes Research 37 (2011) 142–147
Contents lists available at ScienceDirect
Journal of Great Lakes Research j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / j g l r
Use of semipermeable membrane devices to investigate the impacts of DDT (Dichlorodiphenyltrichloroethane) in the Holland Marsh environs of the Lake Simcoe watershed (Ontario, Canada) David Lembcke ⁎, April Ansell, Christopher McConnell, Brian Ginn Lake Simcoe Region Conservation Authority, 120 Bayview Parkway, Newmarket, Ontario L3Y 4X1, Canada
a r t i c l e
i n f o
Article history: Received 7 July 2009 Accepted 8 November 2010 Available online 17 February 2011 Communicated by Jennifer Winter Index words: DDT Semipermeable membrane devices SPMD Holland Marsh Lake Simcoe Historical pesticide use
a b s t r a c t In 2004 the Lake Simcoe Region Conservation Authority (LSRCA) initiated a sampling program to examine historic and emerging contaminants throughout the Lake Simcoe watershed. Through the sampling program it was determined that Dichlorodiphenyltrichloroethane (DDT) concentrations in sediment were exceeding the Canadian Environmental Quality Guidelines just downstream of the Holland Marsh. The objective of this study was to investigate the presence of DDT in the waters surrounding the Holland Marsh and examine if the concentrations sampled represented a potential threat to aquatic and terrestrial biota in the Holland Marsh environs. Semipermeable membrane devices were used to determine DDT concentrations at different locations within the Holland Marsh and surrounding waters for a month in 2006, 2007 and 2008. DDT concentrations were compared to fish tissue guidelines where it was found that some sections of the Marsh experience concentrations which have the potential to impact the health of biota in the immediate area. Varying weather conditions between study years revealed the importance of precipitation in transporting DDT through the marsh. Precipitation above or equaling long-term normals occurred in 2006 and 2008 which coincided with higher DDT concentrations than the significantly drier year of 2007. The information gained in this study will play a valuable role for both terrestrial and aquatic ecosystem managers in understanding how historic DDT use in the Holland Marsh may still be affecting this environment and Lake Simcoe today. © 2011 International Association for Great Lakes Research. Published by Elsevier B.V. All rights reserved.
Introduction The Holland Marsh (44.06°N, 70.58°W) is a large (81 km2) wetland complex in the valley between the Holland and Schomberg rivers (Fig. 1), tributaries of Lake Simcoe, the largest (722 km2) lake in south-central Ontario, Canada. Between 1927 and 1930, a 24 km2 area of the Marsh, south of Highway 11 (Bradford, ON) was dyked and drained to make the largest polder agricultural area in Ontario, currently one of this province's most important farming areas, exporting onions, carrots, (LSEMS, 1995) and Asian greens (e.g. bok choy) to markets both locally and internationally. Currently, arable land in the Marsh is maintained through a complex system of canals, dykes and a main pumping station, designed to maintain specific water levels and quickly remove excess water through the Centre Canal where, at the north end of the Marsh, water is pumped into the West Holland River ~10 km south of Lake Simcoe. Two outer canals (North Canal and South Canal) are used to convey water around the Marsh based on precipitation and irrigation requirements. Through
⁎ Corresponding author. Tel.: +1 905 895 1281. E-mail address: [email protected] (D. Lembcke).
this drainage system, water can only exit the Marsh by evaporation or through the pumping station (F. Jonkman, Holland Marsh Drainage Superintendant, pers. comm. 2008). As in other agricultural areas across North America, dichlorodiphenyltrichloroethane (DDT) was commonly used as an insecticide in the Holland Marsh from ~ 1940s–1960s (Miles and Harris, 1978). DDT use was severely restricted in the early 1970s and banned completely in Canada in 1985 (Canadian Council of Ministers of the Environment (CCME), 1999). While this chemical is no longer used in Canada, a major environmental issue around the world is the persistence and transport of DDT, and its metabolites dichlorodiphenyldichloroethane (DDD) and dichlorodiphenyldichloroethane (DDE), within and between ecosystems, and their bioaccumulation in organisms and biomagnifications in higher trophic levels (World Health Organization (WHO), 1989). From 1972 to 1975, water, sediments, fish, and soils in the Holland Marsh were monitored for organophosphorus and organochlorine pesticides, with DDT recorded as the most prevalent (Miles and Harris, 1978; Miles et al., 1978). In these studies it was noted that minimal breakdown of DDT occurred in the organic soils of the Holland Marsh. This monitoring found DDT concentrations in fish, soil, and sediment that exceeded the current Canadian Environmental Quality Guidelines (CEQG) (CCME, 2003) by 2 to 3 orders of magnitude (Miles and Harris, 1978; Miles et al., 1978).
0380-1330/$ – see front matter © 2011 International Association for Great Lakes Research. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.jglr.2011.01.002
D. Lembcke et al. / Journal of Great Lakes Research 37 (2011) 142–147
143
Fig. 1. Map showing locations of study sites for sediment contaminant study (2004) and semi-permeable membrane device (SPMD) deployments (2006–2008) in Holland Marsh and Holland River. Inset shows study area relative to Lake Simcoe, Ontario, Canada.
Continued monitoring of DDT concentrations in the tissues of Lake Simcoe fish has been ongoing since the 1970s through the Ontario Ministry of the Environment and Ontario Ministry of Natural Resources. Generally, DDT concentrations in fish tissues have decreased since the 1970s and since the 1990s have stabilized (Gewurtz et al., 2011). This plateau is likely the result of changes to food webs (e.g. disruption by invasive species such as Dreissenia spp. and Bythotrephes longimanus) and a decline in new DDT sources with current contamination sourced from atmospheric deposition and historic sources (e.g. release from contaminated sediments) (Gewurtz et al., 2011; Stow et al., 1995). In 2004, the Lake Simcoe Region Conservation Authority (LSRCA) initiated a program to examine historic and emerging contaminants throughout the watershed. This program included the sampling of water and sediments in seven subwatersheds of Lake Simcoe which have agricultural land use, to determine if there was DDT contamination from historic sources. Of the sediment samples analyzed, only those from the West Holland River, directly downstream of Holland
Marsh, had detectable DDT concentrations (LSRCA, 2006). Further sediment sampling in Holland Marsh and downstream in the Holland River in 2005 confirmed total-DDT concentrations (11–110 μg/kg) exceeding Canadian guidelines (1.2–7 μg/kg) (Table 1) were present in sediments at the northern end of the marsh, near the outlet to Holland River. Based on these results, it is possible that the marsh is acting as a DDT source to the Holland River and, potentially, to Lake Simcoe. Hydrophobic pollutants, such as DDT, have been found to partition from sediment to the water column where they can bioconcentrate in aquatic organisms (Lau et al., 1989) and biomagnify to higher trophic levels, including terrestrial consumers (CCME, 1999). A variety of species, including white sucker (Catostomus commersoni), northern pike (Esox lucius), and emerald shiner (Notropis atherinoides) are common to Lake Simcoe (Ontario Ministry of Natural Resources, 2009a, 2009b) and are known to migrate up the Holland River to spawn and spend a portion of their juvenile lifecycle (Scott and Crossman, 1998). As there are no barriers to migration between Lake
144
D. Lembcke et al. / Journal of Great Lakes Research 37 (2011) 142–147
Table 1 Sediment analysis results (2004) from Holland Marsh (sites 3 and 4) and Holland River (site 5) showing concentration of DDT, DDE, and DDD, as well as three Canadian guidelines. All data are μg (contaminant) kg− 1. Contaminant
Site 3
Site 4
Site 5
CSeQGsa
PELb
MOE Table 1c
DDT DDE DDD Total-DDT d
11 45 30 86
110 750 1400 2260
18 134 n.d. 152
1.19 1.42 3.54
4.77 6.75 8.51
7 5 8
a CSeQGs — Canadian Sediment Quality Guidelines for the Protection of Aquatic Life (part of Canadian Environmental Quality Guidelines). b PEL — Probable effect level according to CSeQGs (level at which impacts to aquatic ecosystem occurs). c MOE Table 1 Standards for Ontario Ministry of Environment. d Total-DDT is the sum of all forms of DDT and metabolites (DDE and DDD), included for comparison with historic literature where metabolites could not be resolved.
Simcoe and Holland River up to the marsh outlet, these species could serve as a transport mechanism of DDT to both Lake Simcoe, and higher trophic levels including birds and mammals. In addition to trophic acquisition of DDT, this hydrophobic contaminant can be freely dissolved in water and, as such, biologically available for direct uptake by aquatic organisms (Metcalfe et al., 2000). One method of determining the potential for this uptake is to use biomimetic samplers, in this study a lipid compound (triolein) encased in a semi-permeable membrane (Huckins et al., 1993; Bennett et al., 1996). These semi-permeable membrane devices (SPMDs) are excellent screening tools for estimating the exposure of organisms to even small amounts of bioconcentratable compounds (Huckins et al., 2006) and also have the advantages of being relatively inexpensive in terms of construction, analysis, and field labour required. SPMDs have been employed for many contaminant studies such as assessing organic compounds (Bennett et al., 1996; Huckins et al., 1993; Lu and Wang, 2003; Metcalfe et al., 2000), Polycyclic Aromatic Hydrocarbons (PAHs) (Huckins et al., 1999), and Polychlorinated Biphenyls (PCBs) (Meadows et al., 1998). With numerous other examples available in scientific literature SPMDs are increasingly recognized as applicable to not only individual hydrophobic compounds but increasingly to study complex contaminant mixtures in the environment (Huckins et al., 2006). In this study, SPMDs provided a superior sampling strategy over more traditional methods as: (a) water quality and sediment grab samples can produce inconsistent results and are more costly to analyze; (b) Marsh conditions during the time of deployment would restrict the use of bioindicators such as mussels or fish due to low dissolved oxygen content, warm water temperatures, and restrictions in flow conditions interacting with migration, mortality, metabolism, or selectivedepuration of contaminants; (c) conditions of low dissolved oxygen, low flow rates, and warm water temperatures can promote the release of contaminants from the sediments. It was therefore important that the study be conducted in the late summer or early fall and, to ensure consistent methodology across the study area. SPMDs were selected as the uptake medium as they would function at all locations without the confounding factors that traditional biological methods might introduce. The objective of this study was to investigate the presence and distribution of DDT in the waters of the Holland Marsh, including the movement of DDT down the Holland River toward Lake Simcoe, and to examine if the concentrations sampled represented a potential threat to aquatic and terrestrial biota. Methods Site selection and sample collection Based on the results of the 2004/2005 sediment contaminant study (Table 1, sites 3–5 on Fig. 1), a total of seven sites were selected for
deployment of SPMDs. In 2006, SPMDs were deployed at four sites in the Holland Marsh (sites 1–4, Fig. 1) and 300 m north of the marsh outlet (pumphouse) in the Holland River (site 5). In 2007, a second deployment of SPMDs was carried out at sites 2–5 (Fig. 1) (site 1 was not used due to construction in the Marsh) with sites 6–7 added to gauge contaminant transport downriver toward Lake Simcoe. In 2008, a third SPMD deployment targeted sites 4–6, although samples at site 6 were lost due to vandalism. At each site, three SPMDs, filled with one ml of high purity (99%) triolein, were suspended with in a shroud made from 20 cm diameter aluminum stovepipe capped at each end with a perforated aluminum cover. Galvanized stainless steel wire was used to secure the SPMDs in the shroud so that the SPMDs did not touch one another or the shroud. These deployments were suspended ~20–50 cm below the water surface in autumn (October 10–November 7 2006, August 27– September 26 2007, October 1–November 5 2008). To account for weather variation between sites and years, a temperature logger (HOBO Tidbit) was deployed with each SPMD and precipitation was recorded by the LSRCA monitoring program. At the end of each deployment, SPMDs were collected and transported to the lab in amber jars on ice in a cooler. One SPMD was left exposed to the air as a control during deployment and retrieval. Preparation and analysis of SPMDs followed the methodology of Metcalfe et al. (2000): all materials involved in the construction of the units were washed in hexane to remove trace contaminants; SPMDs were rinsed with distilled water to remove biofouling; and SPMDs were dialysed in hexane, passed through anhydrous sodium sulphate, and analyzed using gel permeation chromatography. Lab analyses were carried out by Centre for Alternative Wastewater Treatment at Sir Sandford Fleming College, Lindsay Ontario (2006–2007) and Dr Chris Metcalfe, Institute for Watershed Science, Trent University, Peterborough Ontario (2008). Detection limits for DDT and metabolites was 1.0 ng/ml (triolein). Analysis of total-DDT included all forms and isomers of DDT and its metabolites (i.e. o,p′-DDT, p,p′-DDT, o,p′-DDD, p,p′-DDD, o,p′-DDE, p,p′-DDE). Due to laboratory error, resolution between DDE and DDD was not possible for 2006–2007 samples. As this was an issue of resolution between metabolites it did not affect total-DDT results. Inferring tissue contaminant concentrations from SPMDs and comparison to CCME guidelines In order to place our results in context, data were related to organisms inhabiting the Holland Marsh and Holland River and the Canadian Tissue Residue Guidelines for the Protection of Wildlife Consumers of Aquatic Biota (CCME, 1999). These guidelines apply to the highest aquatic trophic level (i.e. top level fish) and represent a single, maximum concentration of DDT in aquatic biota that would not result in adverse effects on wildlife consuming these aquatic biota (CCME, 1999). The guidelines represent the most sensitive endpoint for fish tissue DDT concentrations (CCME, 1999) as biomagnification effects are much greater in avian and mammalian consumers when compared with aquatic food chains (Huckins et al., 2006). The guideline value for total-DDT is 14.0 μg kg− 1 (diet wet weight) (CCME, 1999). Comparison of recorded SPMD contaminant values to a biotic tissue guideline should be done with caution, however, as the 2004 sediment samples exceeded DDT guidelines there was interest in the potential of these contaminants to be transported from Holland Marsh to Holland River (and Lake Simcoe), and the uptake of contaminants by organisms. We employed conservative methodology to compare SPMD data with potential tissue contaminants by using the full SPMD weight and applying a range to the calculated values, based on tissue uptake rates recorded by other studies (Meadows et al., 1998; Lu and Wang, 2002, 2003). Our data (DDT, DDD, DDE recorded from SPMDs) were multiplied by 0.915 (density of triolein) to account for the 1 mL
D. Lembcke et al. / Journal of Great Lakes Research 37 (2011) 142–147
of triolein used in each SPMD, then divided by 3.2 to adjust for the non-lipid phase of the SPMD. Metcalfe et al. (2000) recognized that a large portion of the analyte is absorbed by the non-lipid phase of the SPMD (Huckins et al., 2006). As it is unrealistic for one method (e.g. SPMDs) to be representative of all organisms (Huckins et al., 2006), a range was calculated to better represent the variation possible in the diversity of fish species present in Holland Marsh and Holland River. Meadows et al. (1998) and Lu and Wang (2002, 2003) noted SPMD wet-weight uptake rates range from 1 to 2.5 times that of fish tissue wet-weight in a fourth trophic level species for PCBs and organochlorine (OC) pesticides (e.g. lindane, aldrin, heptachlor epoxide, hexachlorobenzene, and 4,4′DDT). As such, our ranges were calculated by dividing the adjusted SPMD total-DDT values by 1 (high end of range) and 2.5 (low end) for more realistic comparison to fish tissue guidelines. Resulting values enabled SPMDs to be compared to wet weight CEQG tissue residue guidelines. Temperature logger data was used to confirm that water temperature during SPMD deployment was not significantly different from laboratory studies (Meadows et al., 1998; Lu and Wang, 2003) or between sites and sampling years. Statistical analysis Due to a relatively small sample size, non-parametric Kruskal– Wallis tests were utilized (SPSS, 2005) to determine significant differences between sampling sites within a year. Nemenyi posthoc test was used to determine differences between sites (Zar, 1998). Results and discussion SPMD uptake and sediment DDT concentrations The basis for the current investigation was a 2004 study of legacy contaminants in sediments of the Holland Marsh and Holland River. In 2006–2007, SPMD uptake of total-DDT (Table 2) was proportional to total-DDT recorded in sediments (Table 1) (r2 = 0.51 (2006), r2 = 0.97 (2007)). In 2008, data was only available from two sites due to equipment vandalism, but comparisons between SPMDs and sediment total-DDT are consistent with the two previous deployments. DDT and its metabolites have a high adsorption in humic soils, especially the organic muck found in wetlands (WHO, 1989). The high proportion of DDD relative to DDT and DDE observed in the sediments at Site 4 (Table 1) is consistent with the preferential metabolism of DDT to DDD under anaerobic conditions (reductive chlorination) in muck sediments (Wang, 2008). Under aerobic conditions DDT Table 2 Mean DDT concentrations (ng ml− 1) taken up by semi-permeable membrane devices (SPMDs) from study sites in Holland Marsh (sites 1–4) and Holland River (sites 5–7), 2006–2008. Data in parentheses are standard deviation. Dash — indicates site not used in year, V — indicates SPMD at site was vandalized, n.d. — indicates concentration was below detectable limit of 1.0 ng ml− 1. Year
Contaminant
Study site 1
2
3
4
5
6
7
87.5 (3.7) 5.6 (0.05) –
120.6 (8.2) 28.5 (3.8) 148 (34.6) 7.7 (2.5) 136 (36.4) 4.1 (1.3)
91.5 (4.2) 9.7 (1.2) 95.6 (4.2) 6.7 (2.4) 85.1 (5) 3.7 (0.6)
–
–
8.2 (2.5) V
3.2 (1.1) –
V
–
V
–
V
–
2006
Total-DDT
2007
Total-DDT
11.1 (10.2) –
2008
Total-DDT
–
29.2 (3) 2.6 (2.5) –
DDT
–
–
–
DDE
–
–
–
DDD
–
–
–
145
typically oxidizes to DDE which is the most stable as well as more toxic and bioaccumulative metabolite of DDT (WHO, 1989; Wang, 2008), thus explaining its relatively higher concentration in the SPMDs. The high proportion of DDD and DDE metabolites to DDT in sediments (Table 1) and SPMDs (Table 2) suggest that the DDT is of historic origin. Variation between study sites Between 2006 and 2007 (Table 2) there was significant variation between the sites (H = 12.9, p b 0.05 and Chi-square (χ2) = 15.83, p b 0.05, respectively), with site 4 having higher concentrations of total-DDT than site 1 (q = 4.65, p b 0.05). Site 4 is located at the outlet the marsh and would have the greatest exposure to materials released from marsh soils due to water level, and changing agricultural management practices, compared to site 1 which has less exposure due to a very small area of the Marsh in the catchment area. In 2007, SPMDs at site 4 recorded higher concentrations of total-DDT (Table 2) than site 2 (q = 4.11, p b 0.05) or site 7 (q = 4.22, p b 0.05). Interestingly, these two sites (sites 2 and 7) are located at the most upstream and downstream ends of the study area, indicating that the highest concentrations of DDT occur between these two sites, at Site 4. In 2008, there was no significant difference between sites (χ2 = 3.857, p N 0.05). Throughout this study, the highest total-DDT concentration in SPMDs was consistently recorded at site 4 followed by sites 5 and 3 (Table 2). This correlates (r = 0.99) with our 2004 sediment study which recorded the highest total-DDT concentrations at site 4 (2260 μg/kg), followed by site 5 (152 μg/kg), and site 3 (86 μg/kg) (Table 1), all exceeding the CEQG sediment guideline of totalDDT = 4.77 μg/kg. This trend indicates that the sediments are the primary source of DDT to the water column. The presence of DDT at sites 6 and 7 (2007) suggest that downstream movement of the contaminants from marsh to Holland River, and possibly Lake Simcoe is occurring. While these values are relatively very low, this may be the result of low precipitation (see below) in 2007 and average values are much higher. This further indicates that DDT is not confined to the marsh and is easily transported downriver. In fact, there was no significant difference in total-DDT concentrations (p N 0.05) between the site 4 (in Holland Marsh) and site 5 (West Holland River). Although dykes and other structures act as a physical barrier, the pumping of water (up to 330 m3/min) is transporting contaminants from the Marsh to river. Variation between years The most notable environmental difference between deployment years was the amount of precipitation: 2007 being an unusually dry year (504 mm total rainfall) while 2006 (869 mm) and 2008 (808 mm) were close to the 30-year normal value (815 mm). In addition, the months prior to SPMD deployment in 2006 mostly exceeded 30-year monthly means with amounts close to regional records set during hurricanes Hazel (1954) and Katie (1955) (Saunders, 2006). Conversely, 2007 was unusually dry with precipitation amounts close to half the 30-year normal for the month of deployment (September) and an overall low annual total (Table 3). The hydrology of the Marsh is artificially regulated by dykes and pumphouses with water movement occurring only when pumps are activated. In 2007 the main pumphouse did not activate through the month of deployment. Conversely in 2006 the pumphouse recorded 951 cumulative pumping hours in response to the above average precipitation (F. Jonkman, Holland Marsh Drainage Superintendant, pers. comm. 2008). As such the SPMDs located at Site 4 and 5 would have been exposed to virtually no flow in 2007 as compared to 2006 and 2008.
146
D. Lembcke et al. / Journal of Great Lakes Research 37 (2011) 142–147
Table 3 Total precipitation (mm) recorded by month with annual total at Bradford, Ontario (2006–2008) (LSRCA, 2008). 30-year normal is included (Environment Canada 2001), months of equipment deployment are in bold.
2006 2007 2008 Norm
Jan
Feb
Mar
April
May
June
July
Aug
Sept
Oct
Nov
Dec
Year Total
55.2 31 51 53.9
67.5 12 69.3 44.4
42.1 31 69 55
90.9 44 51.4 62.8
101 56 86 72
52.4 29.6 63.2 75.1
94.4 29 88.2 87.8
38 32 85 88.6
103.6 40.8 83.6 83.3
100.2 68 32.6 69.5
58 63.4 74.4 68.4
66 67 54 54.5
869.3 503.8 807.7 815.4
Precipitation effects are reflected in recorded SPMD uptake with 2007 having low total-DDT (e.g. site 4=28.5 ng/ml) and 2006/2008 having higher values (site 4 = 120.6 ng/ml and 143.0 ng/ml respectively) (Table 2). Increases in precipitation have been recognized in other studies (e.g. Pham et al., 1996) as being a key agent in the transport of large amounts of DDT from contaminated soils to receiving watercourses. Performance reference compounds are used in some studies to compensate for the effect of increased temperature causing increased contaminant uptake by SPMDs (Rantalainen et al., 2000), however, Huckins et al. (1999) concluded these effects are relatively small and the more important consideration being temperature variation between sites (Huckins et al., 2006). In our study, temperature loggers were deployed with each SPMD unit in place of more expensive performance reference compounds to account for potential temperature effects. Variation between sites in 2006 and 2008 was b1 °C with a mean temperature of 7.6 °C in 2006 and 9.8 °C in 2008. In 2007, variation between sites was 3.5 °C with a mean temperature of 19.9 °C. While Huckins et al. (2006) suggested this variation between sites to be important, the effect on SPMD uptake rates is not significant if temperature differences are b10 °C (Booij et al., 2003). The maximum temperature difference between years was 2007 being 12.3 °C warmer relative to 2006, however a potential increased uptake under warmer conditions was likely mitigated by decreased precipitation. The temperature range for all three years is consistent with the Lu and Wang (2003) and Meadows et al. (1998), studies used to estimate the total-DDT tissue residue ranges for this study. Comparison to DDT tissue residue guideline DDT and its metabolites, as well as many other contaminants have both a bioaccumulative and biomagnification nature in organisms. The Canadian Environmental Quality Guideline (CEQG) accounts for effects of DDT on consumers of aquatic biota (including birds and mammals) and for the protection of wildlife. These guidelines are recommended to be applied to the highest aquatic trophic level which will then account for bioaccumulation by piscivores prior to their predation by avian or mammalian species (CCME, 1999). This is a key point as avian and mammalian species represent the most sensitive endpoint for fish tissue DDT concentrations (CCME, 1999) as biomagnification effects are much greater in avian and mammalian consumers when compared with aquatic food chains (Huckins et al., 2006). Fish sampling data from 1976 in the South Canal of the Holland Marsh recorded fish species from all trophic levels (Ontario Ministry of Natural Resources, 1976) including piscivores and species consumed by other fish, birds, and mammals. Since these investigations, little has changed in the fish community with the waterways of the Holland Marsh, and the Holland River, supporting an intensive recreational fishery. Significant wetland habitat along the Holland River supports a number of sensitive avian and mammalian fish consumers including Bald Eagles (Haliaeetus leucocephalus), a species of concern, and Least Bittern (Ixobrychus exilis) a threatened species (C. Deschamps, LSRCA Senior Natural Heritage Biologist, pers. comm. 2009). To calculate the range of total-DDT tissue residue from SPMD results for comparison to CEQG guidelines (Fig. 2, Table 1), uptake rates for piscivore species in other studies (Lu and Wang, 2002, 2003) were used. This enables the total-DDT bioaccumulation potential of a fourth trophic-
level species to be inferred, but does not account for the biomagnification potential. Biomagnification occurs through the ingestion of tissues containing DDT, a trait SPMDs cannot replicate. While biomagnification is not relevant at lower aquatic trophic levels, it can have deleterious effects at higher levels. Biomagnification, typically low in freshwater food chains, can account for 1 to 3 times the bioconcentration factor in avian and mammalian species (Huckins et al., 2006). The DDT concentrations measured in the SPMDs indicated potential for impacts on aquatic biota when expressed as fish tissue concentrations. In comparison to the CEQG total-DDT guideline of 14 μg/kg, the ranges at sites 3, 4, and 5 (2006) and sites 4 and 5 (2008) inferred total-DDT concentrations in fish tissue that exceeded recommendations (Fig. 2). Although SPMD values are comparable but not identical to actual fish tissue concentrations, they indicate DDT concentrations at some sites in the Holland Marsh and Holland River are of concern and have the potential to impact biota. Coupled with the downstream movement of DDT concentrations out of the Marsh is the upstream migration of a number of fish species. These species spend a portion of their lifecycle in the waters around the Holland Marsh where the higher DDT concentrations were observed, as well as a portion in Lake Simcoe. Both these factors may be involved in the plateau of fish tissue concentrations observed by Gewurtz et al. (2011) as opposed to a continuing decline. As none of the other Lake Simcoe tributaries that were sampled in 2004 detected any DDT concentrations, this suggests the Marsh may be acting as a source of legacy DDT contamination to the immediate environs and potentially Lake Simcoe as well. Future studies with SPMDs should include conventional fish tissue sampling at key sites to determine the full extent of impacts from DDT and its metabolites. Conclusions Monitoring of DDT and its metabolites in sediments and, in the water column through the use of SPMDs, has recorded increased
Fig. 2. Ranges of estimated total-DDT concentration (μg/ kg− 1 wet weight) in fish tissue inferred from total-DDT recorded from semi-permeable membrane devices (SPMD) in Holland Marsh and Holland River (2006–2008) in relation to Canadian Environmental Quality (CEQG) DDT guidelines.
D. Lembcke et al. / Journal of Great Lakes Research 37 (2011) 142–147
concentrations that exceed Canadian guidelines in both the Holland Marsh (sites 3 and 4) and the West Holland River (site 5). Further analysis shows a relatively high proportion of metabolites (DDD, DDE) compared to DDT which indicates a legacy source for this contamination. The three sites of high sediment DDT concentration also correspond to the highest uptake of DDT by SPMDs, signifying the movement of contaminants from sediment to the water column and into aquatic organisms. The main driver of DDT transport is precipitation and, as a result, river flow. During years with precipitation close to the 30-year normal (i.e. 2006, 2008), SPMDs recorded a large uptake of DDT from surrounding water. While the in-water concentration of DDT was likely diluted due to rainfall, the movement of large volumes of water past the SPMDs resulted in a large exposure to the contaminant. In years with low precipitation (i.e. 2007), much less DDT was present in SPMDs and, while the contaminants would have a higher concentration in the surrounding water relative to 2006 and 2008, little water movement would have limited exposure to DDT and thus uptake by SPMDs. Conversion of our SPMD data to fish tissue equivalents indicates that during years of average (or above) precipitation, enough DDT can be taken up by fish tissues to exceed Canadian guidelines for higher trophic levels in aquatic ecosystems, thus posing a risk from legacy contaminants to consumers of these fish species (e.g. birds and mammals) both near the source of contaminant release, and further downriver to Lake Simcoe. Acknowledgments We wish to thank Brent Wootton, Chris Metcalfe and Tracy Metcalfe for their help with SPMD construction and deployment protocols, sample analysis, and helpful comments regarding our methodology. We also thank Art Janse and Frank Jonkman for their assistance in understanding the dynamics of the Holland Marsh drainage system and allowing us access to the Pumphouse. Thanks also to Rob Wilson and Chandler Eves for their field assistance. Ben Longstaff and two anonymous reviewers provided helpful insights that improved the quality of this manuscript. References Bennett, E.R., Metcalfe, C.D., Metcalfe, T.L., 1996. Semi-permeable membrane devices (SPMDs) for monitoring organic contaminants in the Otonabee River, Ontario. Chemosphere 33, 363–375. Booij, K., Hofmans, H.E., Fischer, C.V., Van Weerlee, E.M., 2003. Temperature-dependent uptake rates of nonpolar organic compounds by Semipermeable Membrane Devices and low-density polyethylene membranes. Environ. Sci. Technol. 37, 361–366. Canadian Council of Ministers of the Environment (CCME), 1999. Canadian tissue residue guidelines for the protection of wildlife consumers of aquatic biota: DDT (total). Canadian Environmental Quality Guidelines, 1999. Canadian Council of Ministers of the Environment, Winnipeg. Canadian Council of Ministers of the Environment (CCME), 2003. Summary of existing Canadian Environmental Quality Guidelines. Canadian Environmental Quality Guidelines Summary Table, 2003. Canadian Council of Ministers of the Environment, Winnipeg. Environment Canada, 2001. http://www.climate.weatheroffice.ec.gc.ca/Welcome_e. html2001.
147
Huckins, J.N., Manueera, G.K., Petty, J.D., Mackay, D., Lebo, J.A., 1993. Lipid-containing semipermeable membrane devices for monitoring organic contaminants in water. Environ. Sci. Technol. 27, 2489–2496. Huckins, J., Petty, J.D., Orazio, C.E., Lebo, J.A., Clark, R.C., Gibson, V.L., Gala, W.R., Echols, K. R., 1999. Determination of uptake kinetics (sampling rates) by lipid-containing Semipermeable Membrane Devices (SPMDs) for Polyciclic Aromatic Hydrocarbons (PAHs) in water. Environ. Sci. Technol. 33, 3918–3923. Huckins, J., Petty, J., Booij, Kees, 2006. Monitors of Organic Chemicals in the Environment; Semipermeable Membrane Devices. Springer Science and Business Media. Gewurtz, S.B., Bhavsar, S.P., Jackson, D.A., Awad, E., Winter, J.G., Kolic, T.M., Reiner, E.J., Moody, R., Fletcher, R., 2011. Trends of legacy and emerging-issue contaminants in Lake Simcoe fishes. 37 (Supplement 3), 148–159. Lake Simcoe Environmental Management Strategy (LSEMS), 1995. Lake Simcoe: Our Waters, Our Heritage. Lake Simcoe Region Conservation Authority (LSRCA), 2006. Lake Simcoe Watershed Toxic Pollutant Screening Program. Lake Simcoe Region Conservation Authority (LSRCA), 2008. 2007 Environmental Monitoring Report. Lau, Y.L., Oliver, B.G., Krishnappan, B.G., 1989. Transport of some chlorinated contaminants by the water, suspended sediments, and bed sediments in the St. Clair and Detroit rivers. Environ. Toxicol. Chem. 8 (4), 293–301. Lu, Y., Wang, Z., 2002. Bioconcentration of trace organochlorine pesticides by the rainbow trout. J. Environ. Sci. Health A37 (4), 529–539. Lu, Y., Wang, Z., 2003. Accumulation of Organochlorinated pesticides by trioleincontaining semipermeable membrane device (triolein-SPMD) and rainbow trout. Water Res. 37, 2419–2425. Meadows, J.C., Echols, K.R., Huckins, J.N., Borsuk, F.A., Carline, R.F., Tillitt, D.E., 1998. Estimation of uptake rate constants for PCB congeners accumulated by semipermeable membrane devices and brown trout (Salmo trutta). Environ. Sci. Technol. 32, 1847–1852. Metcalfe, T.L., Metcalfe, C.D., Bennett, E.R., Haffner, G.D., 2000. Distribution of toxic organic contaminants in water and sediments in the Detroit River. J. Great Lakes Res. 26 (1), 55–64. Miles, J.R.W., Harris, C.R., 1978. Insecticide residues in water, sediment, and fish of the drainage system of the Holland Marsh, Ontario, Canada, 1972–75. J. Econ. Entomol. 71, 125–131. Miles, J.R.W., Harris, C.R., Moy, P., 1978. Insecticide residues in organic soil of the Holland Marsh, Ontario, Canada, 1972–1975. J. Econ. Entomol. 71, 97–101. Ontario Ministry of Natural Resouces (MNR), 1976. Fish Sample Data. Ontario Ministry of Natural Resources, 2009a. List of Fish Species found in Lake Simcoe including their Origin, Present Abundance and Abundance Trends as of 2008. Unpublished. Ontario Ministry of Natural Resources, 2009b. Species at Risk in Ontario List. http:// www.mnr.gov.on.ca/en/Business/Species/2ColumnSubPage/276722.html. Pham, T., Lum, K., Lemieux, C., 1996. Seasonal variation of DDT and its metabolites in the St. Lawrence River (Canada) and four of its tributaries. Sci. Total Environ. 179, 17–26. Rantalainen, A., Cretney, W.J., Ikonomou, M.G., 2000. Uptake rates of semipermeable membrane devices (SPMDs) for PCDDs, PCDFs and PCBs in water and sediment. Chemosphere 40, 147–158. Saunders, J., 2006. http://www.on.ec.gc.ca/announce.cfm?ID=766&Lang=e2006. Scott, W.B., Crossman, E.J., 1998. Freshwater Fishes of Canada. Galt House Publications Ltd. SPSS Inc., 2005. SPSS 14.0 Brief Guide. SPSS Inc., Chicago, IL. Stow, C.A., Carpenter, S.R., Eby, L.A., Amrhein, J.F., Hesselberg, R.J., 1995. Evidence that PCBs are approaching stable concentrations in Lake Michigan fishes. Ecol. Appl. 5, 248–260. Wang, H. 2008. Plant growth-promoting rhizobacteria (PGPR) enhanced phytoremediation of DDT contaminated soil. MSc Thesis. Dept. of Biology, University of Waterloo. 117p. WHO (World Health Organization), 1989. DDT and its derivatives: environmental aspects. World Health Organization, United Nations Environmental Programme: EHC, 83. 98p. Zar, J.H., 1998. Biostatistical Analysis, 4th ed. Prentice Hall, Upper Saddle River, New Jersey.
Contents lists available at ScienceDirect
Journal of Great Lakes Research j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / j g l r
Use of semipermeable membrane devices to investigate the impacts of DDT (Dichlorodiphenyltrichloroethane) in the Holland Marsh environs of the Lake Simcoe watershed (Ontario, Canada) David Lembcke ⁎, April Ansell, Christopher McConnell, Brian Ginn Lake Simcoe Region Conservation Authority, 120 Bayview Parkway, Newmarket, Ontario L3Y 4X1, Canada
a r t i c l e
i n f o
Article history: Received 7 July 2009 Accepted 8 November 2010 Available online 17 February 2011 Communicated by Jennifer Winter Index words: DDT Semipermeable membrane devices SPMD Holland Marsh Lake Simcoe Historical pesticide use
a b s t r a c t In 2004 the Lake Simcoe Region Conservation Authority (LSRCA) initiated a sampling program to examine historic and emerging contaminants throughout the Lake Simcoe watershed. Through the sampling program it was determined that Dichlorodiphenyltrichloroethane (DDT) concentrations in sediment were exceeding the Canadian Environmental Quality Guidelines just downstream of the Holland Marsh. The objective of this study was to investigate the presence of DDT in the waters surrounding the Holland Marsh and examine if the concentrations sampled represented a potential threat to aquatic and terrestrial biota in the Holland Marsh environs. Semipermeable membrane devices were used to determine DDT concentrations at different locations within the Holland Marsh and surrounding waters for a month in 2006, 2007 and 2008. DDT concentrations were compared to fish tissue guidelines where it was found that some sections of the Marsh experience concentrations which have the potential to impact the health of biota in the immediate area. Varying weather conditions between study years revealed the importance of precipitation in transporting DDT through the marsh. Precipitation above or equaling long-term normals occurred in 2006 and 2008 which coincided with higher DDT concentrations than the significantly drier year of 2007. The information gained in this study will play a valuable role for both terrestrial and aquatic ecosystem managers in understanding how historic DDT use in the Holland Marsh may still be affecting this environment and Lake Simcoe today. © 2011 International Association for Great Lakes Research. Published by Elsevier B.V. All rights reserved.
Introduction The Holland Marsh (44.06°N, 70.58°W) is a large (81 km2) wetland complex in the valley between the Holland and Schomberg rivers (Fig. 1), tributaries of Lake Simcoe, the largest (722 km2) lake in south-central Ontario, Canada. Between 1927 and 1930, a 24 km2 area of the Marsh, south of Highway 11 (Bradford, ON) was dyked and drained to make the largest polder agricultural area in Ontario, currently one of this province's most important farming areas, exporting onions, carrots, (LSEMS, 1995) and Asian greens (e.g. bok choy) to markets both locally and internationally. Currently, arable land in the Marsh is maintained through a complex system of canals, dykes and a main pumping station, designed to maintain specific water levels and quickly remove excess water through the Centre Canal where, at the north end of the Marsh, water is pumped into the West Holland River ~10 km south of Lake Simcoe. Two outer canals (North Canal and South Canal) are used to convey water around the Marsh based on precipitation and irrigation requirements. Through
⁎ Corresponding author. Tel.: +1 905 895 1281. E-mail address: [email protected] (D. Lembcke).
this drainage system, water can only exit the Marsh by evaporation or through the pumping station (F. Jonkman, Holland Marsh Drainage Superintendant, pers. comm. 2008). As in other agricultural areas across North America, dichlorodiphenyltrichloroethane (DDT) was commonly used as an insecticide in the Holland Marsh from ~ 1940s–1960s (Miles and Harris, 1978). DDT use was severely restricted in the early 1970s and banned completely in Canada in 1985 (Canadian Council of Ministers of the Environment (CCME), 1999). While this chemical is no longer used in Canada, a major environmental issue around the world is the persistence and transport of DDT, and its metabolites dichlorodiphenyldichloroethane (DDD) and dichlorodiphenyldichloroethane (DDE), within and between ecosystems, and their bioaccumulation in organisms and biomagnifications in higher trophic levels (World Health Organization (WHO), 1989). From 1972 to 1975, water, sediments, fish, and soils in the Holland Marsh were monitored for organophosphorus and organochlorine pesticides, with DDT recorded as the most prevalent (Miles and Harris, 1978; Miles et al., 1978). In these studies it was noted that minimal breakdown of DDT occurred in the organic soils of the Holland Marsh. This monitoring found DDT concentrations in fish, soil, and sediment that exceeded the current Canadian Environmental Quality Guidelines (CEQG) (CCME, 2003) by 2 to 3 orders of magnitude (Miles and Harris, 1978; Miles et al., 1978).
0380-1330/$ – see front matter © 2011 International Association for Great Lakes Research. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.jglr.2011.01.002
D. Lembcke et al. / Journal of Great Lakes Research 37 (2011) 142–147
143
Fig. 1. Map showing locations of study sites for sediment contaminant study (2004) and semi-permeable membrane device (SPMD) deployments (2006–2008) in Holland Marsh and Holland River. Inset shows study area relative to Lake Simcoe, Ontario, Canada.
Continued monitoring of DDT concentrations in the tissues of Lake Simcoe fish has been ongoing since the 1970s through the Ontario Ministry of the Environment and Ontario Ministry of Natural Resources. Generally, DDT concentrations in fish tissues have decreased since the 1970s and since the 1990s have stabilized (Gewurtz et al., 2011). This plateau is likely the result of changes to food webs (e.g. disruption by invasive species such as Dreissenia spp. and Bythotrephes longimanus) and a decline in new DDT sources with current contamination sourced from atmospheric deposition and historic sources (e.g. release from contaminated sediments) (Gewurtz et al., 2011; Stow et al., 1995). In 2004, the Lake Simcoe Region Conservation Authority (LSRCA) initiated a program to examine historic and emerging contaminants throughout the watershed. This program included the sampling of water and sediments in seven subwatersheds of Lake Simcoe which have agricultural land use, to determine if there was DDT contamination from historic sources. Of the sediment samples analyzed, only those from the West Holland River, directly downstream of Holland
Marsh, had detectable DDT concentrations (LSRCA, 2006). Further sediment sampling in Holland Marsh and downstream in the Holland River in 2005 confirmed total-DDT concentrations (11–110 μg/kg) exceeding Canadian guidelines (1.2–7 μg/kg) (Table 1) were present in sediments at the northern end of the marsh, near the outlet to Holland River. Based on these results, it is possible that the marsh is acting as a DDT source to the Holland River and, potentially, to Lake Simcoe. Hydrophobic pollutants, such as DDT, have been found to partition from sediment to the water column where they can bioconcentrate in aquatic organisms (Lau et al., 1989) and biomagnify to higher trophic levels, including terrestrial consumers (CCME, 1999). A variety of species, including white sucker (Catostomus commersoni), northern pike (Esox lucius), and emerald shiner (Notropis atherinoides) are common to Lake Simcoe (Ontario Ministry of Natural Resources, 2009a, 2009b) and are known to migrate up the Holland River to spawn and spend a portion of their juvenile lifecycle (Scott and Crossman, 1998). As there are no barriers to migration between Lake
144
D. Lembcke et al. / Journal of Great Lakes Research 37 (2011) 142–147
Table 1 Sediment analysis results (2004) from Holland Marsh (sites 3 and 4) and Holland River (site 5) showing concentration of DDT, DDE, and DDD, as well as three Canadian guidelines. All data are μg (contaminant) kg− 1. Contaminant
Site 3
Site 4
Site 5
CSeQGsa
PELb
MOE Table 1c
DDT DDE DDD Total-DDT d
11 45 30 86
110 750 1400 2260
18 134 n.d. 152
1.19 1.42 3.54
4.77 6.75 8.51
7 5 8
a CSeQGs — Canadian Sediment Quality Guidelines for the Protection of Aquatic Life (part of Canadian Environmental Quality Guidelines). b PEL — Probable effect level according to CSeQGs (level at which impacts to aquatic ecosystem occurs). c MOE Table 1 Standards for Ontario Ministry of Environment. d Total-DDT is the sum of all forms of DDT and metabolites (DDE and DDD), included for comparison with historic literature where metabolites could not be resolved.
Simcoe and Holland River up to the marsh outlet, these species could serve as a transport mechanism of DDT to both Lake Simcoe, and higher trophic levels including birds and mammals. In addition to trophic acquisition of DDT, this hydrophobic contaminant can be freely dissolved in water and, as such, biologically available for direct uptake by aquatic organisms (Metcalfe et al., 2000). One method of determining the potential for this uptake is to use biomimetic samplers, in this study a lipid compound (triolein) encased in a semi-permeable membrane (Huckins et al., 1993; Bennett et al., 1996). These semi-permeable membrane devices (SPMDs) are excellent screening tools for estimating the exposure of organisms to even small amounts of bioconcentratable compounds (Huckins et al., 2006) and also have the advantages of being relatively inexpensive in terms of construction, analysis, and field labour required. SPMDs have been employed for many contaminant studies such as assessing organic compounds (Bennett et al., 1996; Huckins et al., 1993; Lu and Wang, 2003; Metcalfe et al., 2000), Polycyclic Aromatic Hydrocarbons (PAHs) (Huckins et al., 1999), and Polychlorinated Biphenyls (PCBs) (Meadows et al., 1998). With numerous other examples available in scientific literature SPMDs are increasingly recognized as applicable to not only individual hydrophobic compounds but increasingly to study complex contaminant mixtures in the environment (Huckins et al., 2006). In this study, SPMDs provided a superior sampling strategy over more traditional methods as: (a) water quality and sediment grab samples can produce inconsistent results and are more costly to analyze; (b) Marsh conditions during the time of deployment would restrict the use of bioindicators such as mussels or fish due to low dissolved oxygen content, warm water temperatures, and restrictions in flow conditions interacting with migration, mortality, metabolism, or selectivedepuration of contaminants; (c) conditions of low dissolved oxygen, low flow rates, and warm water temperatures can promote the release of contaminants from the sediments. It was therefore important that the study be conducted in the late summer or early fall and, to ensure consistent methodology across the study area. SPMDs were selected as the uptake medium as they would function at all locations without the confounding factors that traditional biological methods might introduce. The objective of this study was to investigate the presence and distribution of DDT in the waters of the Holland Marsh, including the movement of DDT down the Holland River toward Lake Simcoe, and to examine if the concentrations sampled represented a potential threat to aquatic and terrestrial biota. Methods Site selection and sample collection Based on the results of the 2004/2005 sediment contaminant study (Table 1, sites 3–5 on Fig. 1), a total of seven sites were selected for
deployment of SPMDs. In 2006, SPMDs were deployed at four sites in the Holland Marsh (sites 1–4, Fig. 1) and 300 m north of the marsh outlet (pumphouse) in the Holland River (site 5). In 2007, a second deployment of SPMDs was carried out at sites 2–5 (Fig. 1) (site 1 was not used due to construction in the Marsh) with sites 6–7 added to gauge contaminant transport downriver toward Lake Simcoe. In 2008, a third SPMD deployment targeted sites 4–6, although samples at site 6 were lost due to vandalism. At each site, three SPMDs, filled with one ml of high purity (99%) triolein, were suspended with in a shroud made from 20 cm diameter aluminum stovepipe capped at each end with a perforated aluminum cover. Galvanized stainless steel wire was used to secure the SPMDs in the shroud so that the SPMDs did not touch one another or the shroud. These deployments were suspended ~20–50 cm below the water surface in autumn (October 10–November 7 2006, August 27– September 26 2007, October 1–November 5 2008). To account for weather variation between sites and years, a temperature logger (HOBO Tidbit) was deployed with each SPMD and precipitation was recorded by the LSRCA monitoring program. At the end of each deployment, SPMDs were collected and transported to the lab in amber jars on ice in a cooler. One SPMD was left exposed to the air as a control during deployment and retrieval. Preparation and analysis of SPMDs followed the methodology of Metcalfe et al. (2000): all materials involved in the construction of the units were washed in hexane to remove trace contaminants; SPMDs were rinsed with distilled water to remove biofouling; and SPMDs were dialysed in hexane, passed through anhydrous sodium sulphate, and analyzed using gel permeation chromatography. Lab analyses were carried out by Centre for Alternative Wastewater Treatment at Sir Sandford Fleming College, Lindsay Ontario (2006–2007) and Dr Chris Metcalfe, Institute for Watershed Science, Trent University, Peterborough Ontario (2008). Detection limits for DDT and metabolites was 1.0 ng/ml (triolein). Analysis of total-DDT included all forms and isomers of DDT and its metabolites (i.e. o,p′-DDT, p,p′-DDT, o,p′-DDD, p,p′-DDD, o,p′-DDE, p,p′-DDE). Due to laboratory error, resolution between DDE and DDD was not possible for 2006–2007 samples. As this was an issue of resolution between metabolites it did not affect total-DDT results. Inferring tissue contaminant concentrations from SPMDs and comparison to CCME guidelines In order to place our results in context, data were related to organisms inhabiting the Holland Marsh and Holland River and the Canadian Tissue Residue Guidelines for the Protection of Wildlife Consumers of Aquatic Biota (CCME, 1999). These guidelines apply to the highest aquatic trophic level (i.e. top level fish) and represent a single, maximum concentration of DDT in aquatic biota that would not result in adverse effects on wildlife consuming these aquatic biota (CCME, 1999). The guidelines represent the most sensitive endpoint for fish tissue DDT concentrations (CCME, 1999) as biomagnification effects are much greater in avian and mammalian consumers when compared with aquatic food chains (Huckins et al., 2006). The guideline value for total-DDT is 14.0 μg kg− 1 (diet wet weight) (CCME, 1999). Comparison of recorded SPMD contaminant values to a biotic tissue guideline should be done with caution, however, as the 2004 sediment samples exceeded DDT guidelines there was interest in the potential of these contaminants to be transported from Holland Marsh to Holland River (and Lake Simcoe), and the uptake of contaminants by organisms. We employed conservative methodology to compare SPMD data with potential tissue contaminants by using the full SPMD weight and applying a range to the calculated values, based on tissue uptake rates recorded by other studies (Meadows et al., 1998; Lu and Wang, 2002, 2003). Our data (DDT, DDD, DDE recorded from SPMDs) were multiplied by 0.915 (density of triolein) to account for the 1 mL
D. Lembcke et al. / Journal of Great Lakes Research 37 (2011) 142–147
of triolein used in each SPMD, then divided by 3.2 to adjust for the non-lipid phase of the SPMD. Metcalfe et al. (2000) recognized that a large portion of the analyte is absorbed by the non-lipid phase of the SPMD (Huckins et al., 2006). As it is unrealistic for one method (e.g. SPMDs) to be representative of all organisms (Huckins et al., 2006), a range was calculated to better represent the variation possible in the diversity of fish species present in Holland Marsh and Holland River. Meadows et al. (1998) and Lu and Wang (2002, 2003) noted SPMD wet-weight uptake rates range from 1 to 2.5 times that of fish tissue wet-weight in a fourth trophic level species for PCBs and organochlorine (OC) pesticides (e.g. lindane, aldrin, heptachlor epoxide, hexachlorobenzene, and 4,4′DDT). As such, our ranges were calculated by dividing the adjusted SPMD total-DDT values by 1 (high end of range) and 2.5 (low end) for more realistic comparison to fish tissue guidelines. Resulting values enabled SPMDs to be compared to wet weight CEQG tissue residue guidelines. Temperature logger data was used to confirm that water temperature during SPMD deployment was not significantly different from laboratory studies (Meadows et al., 1998; Lu and Wang, 2003) or between sites and sampling years. Statistical analysis Due to a relatively small sample size, non-parametric Kruskal– Wallis tests were utilized (SPSS, 2005) to determine significant differences between sampling sites within a year. Nemenyi posthoc test was used to determine differences between sites (Zar, 1998). Results and discussion SPMD uptake and sediment DDT concentrations The basis for the current investigation was a 2004 study of legacy contaminants in sediments of the Holland Marsh and Holland River. In 2006–2007, SPMD uptake of total-DDT (Table 2) was proportional to total-DDT recorded in sediments (Table 1) (r2 = 0.51 (2006), r2 = 0.97 (2007)). In 2008, data was only available from two sites due to equipment vandalism, but comparisons between SPMDs and sediment total-DDT are consistent with the two previous deployments. DDT and its metabolites have a high adsorption in humic soils, especially the organic muck found in wetlands (WHO, 1989). The high proportion of DDD relative to DDT and DDE observed in the sediments at Site 4 (Table 1) is consistent with the preferential metabolism of DDT to DDD under anaerobic conditions (reductive chlorination) in muck sediments (Wang, 2008). Under aerobic conditions DDT Table 2 Mean DDT concentrations (ng ml− 1) taken up by semi-permeable membrane devices (SPMDs) from study sites in Holland Marsh (sites 1–4) and Holland River (sites 5–7), 2006–2008. Data in parentheses are standard deviation. Dash — indicates site not used in year, V — indicates SPMD at site was vandalized, n.d. — indicates concentration was below detectable limit of 1.0 ng ml− 1. Year
Contaminant
Study site 1
2
3
4
5
6
7
87.5 (3.7) 5.6 (0.05) –
120.6 (8.2) 28.5 (3.8) 148 (34.6) 7.7 (2.5) 136 (36.4) 4.1 (1.3)
91.5 (4.2) 9.7 (1.2) 95.6 (4.2) 6.7 (2.4) 85.1 (5) 3.7 (0.6)
–
–
8.2 (2.5) V
3.2 (1.1) –
V
–
V
–
V
–
2006
Total-DDT
2007
Total-DDT
11.1 (10.2) –
2008
Total-DDT
–
29.2 (3) 2.6 (2.5) –
DDT
–
–
–
DDE
–
–
–
DDD
–
–
–
145
typically oxidizes to DDE which is the most stable as well as more toxic and bioaccumulative metabolite of DDT (WHO, 1989; Wang, 2008), thus explaining its relatively higher concentration in the SPMDs. The high proportion of DDD and DDE metabolites to DDT in sediments (Table 1) and SPMDs (Table 2) suggest that the DDT is of historic origin. Variation between study sites Between 2006 and 2007 (Table 2) there was significant variation between the sites (H = 12.9, p b 0.05 and Chi-square (χ2) = 15.83, p b 0.05, respectively), with site 4 having higher concentrations of total-DDT than site 1 (q = 4.65, p b 0.05). Site 4 is located at the outlet the marsh and would have the greatest exposure to materials released from marsh soils due to water level, and changing agricultural management practices, compared to site 1 which has less exposure due to a very small area of the Marsh in the catchment area. In 2007, SPMDs at site 4 recorded higher concentrations of total-DDT (Table 2) than site 2 (q = 4.11, p b 0.05) or site 7 (q = 4.22, p b 0.05). Interestingly, these two sites (sites 2 and 7) are located at the most upstream and downstream ends of the study area, indicating that the highest concentrations of DDT occur between these two sites, at Site 4. In 2008, there was no significant difference between sites (χ2 = 3.857, p N 0.05). Throughout this study, the highest total-DDT concentration in SPMDs was consistently recorded at site 4 followed by sites 5 and 3 (Table 2). This correlates (r = 0.99) with our 2004 sediment study which recorded the highest total-DDT concentrations at site 4 (2260 μg/kg), followed by site 5 (152 μg/kg), and site 3 (86 μg/kg) (Table 1), all exceeding the CEQG sediment guideline of totalDDT = 4.77 μg/kg. This trend indicates that the sediments are the primary source of DDT to the water column. The presence of DDT at sites 6 and 7 (2007) suggest that downstream movement of the contaminants from marsh to Holland River, and possibly Lake Simcoe is occurring. While these values are relatively very low, this may be the result of low precipitation (see below) in 2007 and average values are much higher. This further indicates that DDT is not confined to the marsh and is easily transported downriver. In fact, there was no significant difference in total-DDT concentrations (p N 0.05) between the site 4 (in Holland Marsh) and site 5 (West Holland River). Although dykes and other structures act as a physical barrier, the pumping of water (up to 330 m3/min) is transporting contaminants from the Marsh to river. Variation between years The most notable environmental difference between deployment years was the amount of precipitation: 2007 being an unusually dry year (504 mm total rainfall) while 2006 (869 mm) and 2008 (808 mm) were close to the 30-year normal value (815 mm). In addition, the months prior to SPMD deployment in 2006 mostly exceeded 30-year monthly means with amounts close to regional records set during hurricanes Hazel (1954) and Katie (1955) (Saunders, 2006). Conversely, 2007 was unusually dry with precipitation amounts close to half the 30-year normal for the month of deployment (September) and an overall low annual total (Table 3). The hydrology of the Marsh is artificially regulated by dykes and pumphouses with water movement occurring only when pumps are activated. In 2007 the main pumphouse did not activate through the month of deployment. Conversely in 2006 the pumphouse recorded 951 cumulative pumping hours in response to the above average precipitation (F. Jonkman, Holland Marsh Drainage Superintendant, pers. comm. 2008). As such the SPMDs located at Site 4 and 5 would have been exposed to virtually no flow in 2007 as compared to 2006 and 2008.
146
D. Lembcke et al. / Journal of Great Lakes Research 37 (2011) 142–147
Table 3 Total precipitation (mm) recorded by month with annual total at Bradford, Ontario (2006–2008) (LSRCA, 2008). 30-year normal is included (Environment Canada 2001), months of equipment deployment are in bold.
2006 2007 2008 Norm
Jan
Feb
Mar
April
May
June
July
Aug
Sept
Oct
Nov
Dec
Year Total
55.2 31 51 53.9
67.5 12 69.3 44.4
42.1 31 69 55
90.9 44 51.4 62.8
101 56 86 72
52.4 29.6 63.2 75.1
94.4 29 88.2 87.8
38 32 85 88.6
103.6 40.8 83.6 83.3
100.2 68 32.6 69.5
58 63.4 74.4 68.4
66 67 54 54.5
869.3 503.8 807.7 815.4
Precipitation effects are reflected in recorded SPMD uptake with 2007 having low total-DDT (e.g. site 4=28.5 ng/ml) and 2006/2008 having higher values (site 4 = 120.6 ng/ml and 143.0 ng/ml respectively) (Table 2). Increases in precipitation have been recognized in other studies (e.g. Pham et al., 1996) as being a key agent in the transport of large amounts of DDT from contaminated soils to receiving watercourses. Performance reference compounds are used in some studies to compensate for the effect of increased temperature causing increased contaminant uptake by SPMDs (Rantalainen et al., 2000), however, Huckins et al. (1999) concluded these effects are relatively small and the more important consideration being temperature variation between sites (Huckins et al., 2006). In our study, temperature loggers were deployed with each SPMD unit in place of more expensive performance reference compounds to account for potential temperature effects. Variation between sites in 2006 and 2008 was b1 °C with a mean temperature of 7.6 °C in 2006 and 9.8 °C in 2008. In 2007, variation between sites was 3.5 °C with a mean temperature of 19.9 °C. While Huckins et al. (2006) suggested this variation between sites to be important, the effect on SPMD uptake rates is not significant if temperature differences are b10 °C (Booij et al., 2003). The maximum temperature difference between years was 2007 being 12.3 °C warmer relative to 2006, however a potential increased uptake under warmer conditions was likely mitigated by decreased precipitation. The temperature range for all three years is consistent with the Lu and Wang (2003) and Meadows et al. (1998), studies used to estimate the total-DDT tissue residue ranges for this study. Comparison to DDT tissue residue guideline DDT and its metabolites, as well as many other contaminants have both a bioaccumulative and biomagnification nature in organisms. The Canadian Environmental Quality Guideline (CEQG) accounts for effects of DDT on consumers of aquatic biota (including birds and mammals) and for the protection of wildlife. These guidelines are recommended to be applied to the highest aquatic trophic level which will then account for bioaccumulation by piscivores prior to their predation by avian or mammalian species (CCME, 1999). This is a key point as avian and mammalian species represent the most sensitive endpoint for fish tissue DDT concentrations (CCME, 1999) as biomagnification effects are much greater in avian and mammalian consumers when compared with aquatic food chains (Huckins et al., 2006). Fish sampling data from 1976 in the South Canal of the Holland Marsh recorded fish species from all trophic levels (Ontario Ministry of Natural Resources, 1976) including piscivores and species consumed by other fish, birds, and mammals. Since these investigations, little has changed in the fish community with the waterways of the Holland Marsh, and the Holland River, supporting an intensive recreational fishery. Significant wetland habitat along the Holland River supports a number of sensitive avian and mammalian fish consumers including Bald Eagles (Haliaeetus leucocephalus), a species of concern, and Least Bittern (Ixobrychus exilis) a threatened species (C. Deschamps, LSRCA Senior Natural Heritage Biologist, pers. comm. 2009). To calculate the range of total-DDT tissue residue from SPMD results for comparison to CEQG guidelines (Fig. 2, Table 1), uptake rates for piscivore species in other studies (Lu and Wang, 2002, 2003) were used. This enables the total-DDT bioaccumulation potential of a fourth trophic-
level species to be inferred, but does not account for the biomagnification potential. Biomagnification occurs through the ingestion of tissues containing DDT, a trait SPMDs cannot replicate. While biomagnification is not relevant at lower aquatic trophic levels, it can have deleterious effects at higher levels. Biomagnification, typically low in freshwater food chains, can account for 1 to 3 times the bioconcentration factor in avian and mammalian species (Huckins et al., 2006). The DDT concentrations measured in the SPMDs indicated potential for impacts on aquatic biota when expressed as fish tissue concentrations. In comparison to the CEQG total-DDT guideline of 14 μg/kg, the ranges at sites 3, 4, and 5 (2006) and sites 4 and 5 (2008) inferred total-DDT concentrations in fish tissue that exceeded recommendations (Fig. 2). Although SPMD values are comparable but not identical to actual fish tissue concentrations, they indicate DDT concentrations at some sites in the Holland Marsh and Holland River are of concern and have the potential to impact biota. Coupled with the downstream movement of DDT concentrations out of the Marsh is the upstream migration of a number of fish species. These species spend a portion of their lifecycle in the waters around the Holland Marsh where the higher DDT concentrations were observed, as well as a portion in Lake Simcoe. Both these factors may be involved in the plateau of fish tissue concentrations observed by Gewurtz et al. (2011) as opposed to a continuing decline. As none of the other Lake Simcoe tributaries that were sampled in 2004 detected any DDT concentrations, this suggests the Marsh may be acting as a source of legacy DDT contamination to the immediate environs and potentially Lake Simcoe as well. Future studies with SPMDs should include conventional fish tissue sampling at key sites to determine the full extent of impacts from DDT and its metabolites. Conclusions Monitoring of DDT and its metabolites in sediments and, in the water column through the use of SPMDs, has recorded increased
Fig. 2. Ranges of estimated total-DDT concentration (μg/ kg− 1 wet weight) in fish tissue inferred from total-DDT recorded from semi-permeable membrane devices (SPMD) in Holland Marsh and Holland River (2006–2008) in relation to Canadian Environmental Quality (CEQG) DDT guidelines.
D. Lembcke et al. / Journal of Great Lakes Research 37 (2011) 142–147
concentrations that exceed Canadian guidelines in both the Holland Marsh (sites 3 and 4) and the West Holland River (site 5). Further analysis shows a relatively high proportion of metabolites (DDD, DDE) compared to DDT which indicates a legacy source for this contamination. The three sites of high sediment DDT concentration also correspond to the highest uptake of DDT by SPMDs, signifying the movement of contaminants from sediment to the water column and into aquatic organisms. The main driver of DDT transport is precipitation and, as a result, river flow. During years with precipitation close to the 30-year normal (i.e. 2006, 2008), SPMDs recorded a large uptake of DDT from surrounding water. While the in-water concentration of DDT was likely diluted due to rainfall, the movement of large volumes of water past the SPMDs resulted in a large exposure to the contaminant. In years with low precipitation (i.e. 2007), much less DDT was present in SPMDs and, while the contaminants would have a higher concentration in the surrounding water relative to 2006 and 2008, little water movement would have limited exposure to DDT and thus uptake by SPMDs. Conversion of our SPMD data to fish tissue equivalents indicates that during years of average (or above) precipitation, enough DDT can be taken up by fish tissues to exceed Canadian guidelines for higher trophic levels in aquatic ecosystems, thus posing a risk from legacy contaminants to consumers of these fish species (e.g. birds and mammals) both near the source of contaminant release, and further downriver to Lake Simcoe. Acknowledgments We wish to thank Brent Wootton, Chris Metcalfe and Tracy Metcalfe for their help with SPMD construction and deployment protocols, sample analysis, and helpful comments regarding our methodology. We also thank Art Janse and Frank Jonkman for their assistance in understanding the dynamics of the Holland Marsh drainage system and allowing us access to the Pumphouse. Thanks also to Rob Wilson and Chandler Eves for their field assistance. Ben Longstaff and two anonymous reviewers provided helpful insights that improved the quality of this manuscript. References Bennett, E.R., Metcalfe, C.D., Metcalfe, T.L., 1996. Semi-permeable membrane devices (SPMDs) for monitoring organic contaminants in the Otonabee River, Ontario. Chemosphere 33, 363–375. Booij, K., Hofmans, H.E., Fischer, C.V., Van Weerlee, E.M., 2003. Temperature-dependent uptake rates of nonpolar organic compounds by Semipermeable Membrane Devices and low-density polyethylene membranes. Environ. Sci. Technol. 37, 361–366. Canadian Council of Ministers of the Environment (CCME), 1999. Canadian tissue residue guidelines for the protection of wildlife consumers of aquatic biota: DDT (total). Canadian Environmental Quality Guidelines, 1999. Canadian Council of Ministers of the Environment, Winnipeg. Canadian Council of Ministers of the Environment (CCME), 2003. Summary of existing Canadian Environmental Quality Guidelines. Canadian Environmental Quality Guidelines Summary Table, 2003. Canadian Council of Ministers of the Environment, Winnipeg. Environment Canada, 2001. http://www.climate.weatheroffice.ec.gc.ca/Welcome_e. html2001.
147
Huckins, J.N., Manueera, G.K., Petty, J.D., Mackay, D., Lebo, J.A., 1993. Lipid-containing semipermeable membrane devices for monitoring organic contaminants in water. Environ. Sci. Technol. 27, 2489–2496. Huckins, J., Petty, J.D., Orazio, C.E., Lebo, J.A., Clark, R.C., Gibson, V.L., Gala, W.R., Echols, K. R., 1999. Determination of uptake kinetics (sampling rates) by lipid-containing Semipermeable Membrane Devices (SPMDs) for Polyciclic Aromatic Hydrocarbons (PAHs) in water. Environ. Sci. Technol. 33, 3918–3923. Huckins, J., Petty, J., Booij, Kees, 2006. Monitors of Organic Chemicals in the Environment; Semipermeable Membrane Devices. Springer Science and Business Media. Gewurtz, S.B., Bhavsar, S.P., Jackson, D.A., Awad, E., Winter, J.G., Kolic, T.M., Reiner, E.J., Moody, R., Fletcher, R., 2011. Trends of legacy and emerging-issue contaminants in Lake Simcoe fishes. 37 (Supplement 3), 148–159. Lake Simcoe Environmental Management Strategy (LSEMS), 1995. Lake Simcoe: Our Waters, Our Heritage. Lake Simcoe Region Conservation Authority (LSRCA), 2006. Lake Simcoe Watershed Toxic Pollutant Screening Program. Lake Simcoe Region Conservation Authority (LSRCA), 2008. 2007 Environmental Monitoring Report. Lau, Y.L., Oliver, B.G., Krishnappan, B.G., 1989. Transport of some chlorinated contaminants by the water, suspended sediments, and bed sediments in the St. Clair and Detroit rivers. Environ. Toxicol. Chem. 8 (4), 293–301. Lu, Y., Wang, Z., 2002. Bioconcentration of trace organochlorine pesticides by the rainbow trout. J. Environ. Sci. Health A37 (4), 529–539. Lu, Y., Wang, Z., 2003. Accumulation of Organochlorinated pesticides by trioleincontaining semipermeable membrane device (triolein-SPMD) and rainbow trout. Water Res. 37, 2419–2425. Meadows, J.C., Echols, K.R., Huckins, J.N., Borsuk, F.A., Carline, R.F., Tillitt, D.E., 1998. Estimation of uptake rate constants for PCB congeners accumulated by semipermeable membrane devices and brown trout (Salmo trutta). Environ. Sci. Technol. 32, 1847–1852. Metcalfe, T.L., Metcalfe, C.D., Bennett, E.R., Haffner, G.D., 2000. Distribution of toxic organic contaminants in water and sediments in the Detroit River. J. Great Lakes Res. 26 (1), 55–64. Miles, J.R.W., Harris, C.R., 1978. Insecticide residues in water, sediment, and fish of the drainage system of the Holland Marsh, Ontario, Canada, 1972–75. J. Econ. Entomol. 71, 125–131. Miles, J.R.W., Harris, C.R., Moy, P., 1978. Insecticide residues in organic soil of the Holland Marsh, Ontario, Canada, 1972–1975. J. Econ. Entomol. 71, 97–101. Ontario Ministry of Natural Resouces (MNR), 1976. Fish Sample Data. Ontario Ministry of Natural Resources, 2009a. List of Fish Species found in Lake Simcoe including their Origin, Present Abundance and Abundance Trends as of 2008. Unpublished. Ontario Ministry of Natural Resources, 2009b. Species at Risk in Ontario List. http:// www.mnr.gov.on.ca/en/Business/Species/2ColumnSubPage/276722.html. Pham, T., Lum, K., Lemieux, C., 1996. Seasonal variation of DDT and its metabolites in the St. Lawrence River (Canada) and four of its tributaries. Sci. Total Environ. 179, 17–26. Rantalainen, A., Cretney, W.J., Ikonomou, M.G., 2000. Uptake rates of semipermeable membrane devices (SPMDs) for PCDDs, PCDFs and PCBs in water and sediment. Chemosphere 40, 147–158. Saunders, J., 2006. http://www.on.ec.gc.ca/announce.cfm?ID=766&Lang=e2006. Scott, W.B., Crossman, E.J., 1998. Freshwater Fishes of Canada. Galt House Publications Ltd. SPSS Inc., 2005. SPSS 14.0 Brief Guide. SPSS Inc., Chicago, IL. Stow, C.A., Carpenter, S.R., Eby, L.A., Amrhein, J.F., Hesselberg, R.J., 1995. Evidence that PCBs are approaching stable concentrations in Lake Michigan fishes. Ecol. Appl. 5, 248–260. Wang, H. 2008. Plant growth-promoting rhizobacteria (PGPR) enhanced phytoremediation of DDT contaminated soil. MSc Thesis. Dept. of Biology, University of Waterloo. 117p. WHO (World Health Organization), 1989. DDT and its derivatives: environmental aspects. World Health Organization, United Nations Environmental Programme: EHC, 83. 98p. Zar, J.H., 1998. Biostatistical Analysis, 4th ed. Prentice Hall, Upper Saddle River, New Jersey.