Mercury concentration in black flies Simulium spp. (Diptera, Simuliidae) from soft-water streams in Ontario, Canada

Environmental Pollution 143 (2006) 529e535 www.elsevier.com/locate/envpol

Mercury concentration in black flies Simulium spp. (Diptera, Simuliidae) from soft-water streams in Ontario, Canada K.M. Harding, J.A. Gowland, P.J. Dillon* Trent University, 1600 West Bank Drive, Peterborough, ON K9J 7B8, Canada Received 1 June 2005; received in revised form 30 October 2005; accepted 10 November 2005

Accumulation of total mercury by black fly larvae is affected by stream pH, DOC and wetland area in the stream catchment. Abstract Total Hg in Simulium spp. (Diptera, Simuliidae) was measured in 17 soft-water streams in the District of Muskoka and Haliburton County (Ontario, Canada) during 2003 and 2004. Black flies contained 0.07e0.64 mg/g total Hg (dry weight). The methylmercury concentration was measured in 6 samples of the 17, and ranged from 58% to 93% of total Hg. The concentration of total Hg is much higher than has been found in other filter feeding insects, and represents a significant potential source of Hg to fish. Mercury concentrations in Simulium spp. at different sites were strongly positively correlated with dissolved organic carbon, and the proportion of land within each catchment that was wetland. There was also a strong negative correlation with pH. By examining Hg concentration in filter feeding insects we have found a significant entry point for Hg and MeHg into the food web. Ó 2005 Elsevier Ltd. All rights reserved. Keywords: Mercury; Dissolved organic carbon (DOC); Simuliidae; Black fly larvae; Bioavailability

1. Introduction The high Hg concentrations in fish in remote lakes are a concern in Canada, Sweden, and the United States (AMAP, 1998), due to the potential human health effects linked to consumption of fish (Wright and Welbourn, 2002). Fish obtain most of their Hg body burden through their food (Spry and Wiener, 1991; Futter, 1994; Gorski et al., 2003); however, little is known about how Hg becomes incorporated into the lower parts of the food web (Mason et al., 2000). Both acidity and dissolved organic carbon (DOC) have been linked to Hg concentration in fish. Lake and/or stream pH is often negatively correlated with total Hg concentration in water (Kalbitz and Wennrich, 1998), and fish found in acidic conditions often have higher tissue concentrations of

* Corresponding author. Tel.: þ1 705 748 1011x7536; fax: þ1 705 748 1625. E-mail address: [email protected] (P.J. Dillon). 0269-7491/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2005.11.040

total Hg than those from higher pH systems (McMurty et al., 1989; Wren et al., 1991). In natural freshwater, most of the inorganic Hg and methylmercury (MeHg) is bound to DOC (Hintelmann et al., 1997; Haitzer et al., 2002). When Hg binds to DOC, this may increase the bioavailable fraction of Hg and lead to greater bioaccumulation of Hg in organisms. While this has been reported in natural systems by some researchers (McMurty et al., 1989; Driscoll et al., 1995; Westcott and Kalff, 1996), others (Wren et al., 1991) have found the opposite relationship, indicating a need for more research. At present, there have been no studies looking at the change in Hg bioaccumulation when Hg is bound to DOM. Although DOC, pH and other water chemistry parameters are generally correlated with Hg and methylmercury concentrations in fish, these factors may affect fish by altering uptake in other parts of the food web rather than by affecting direct uptake in fish (Watras and Bloom, 1992; Mason et al., 2000). Because black flies (Diptera: Simuliidae) are a significant food source for many fish as larvae (Allan, 1981; Jones

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et al., 2003), and for birds and fish as adults (Davies, 1981; Lindsay and Dimmick, 1983), they are a significant potential point of entry for Hg uptake into the food web. Dissolved organic matter (DOM) is operationally defined as organic matter that passes through a 0.45 mm filter, meaning that it includes both colloidal and true dissolved organic matter (Wetzel, 1983). The carbon content of DOM is around 50e55%, and DOC is often used as a surrogate for DOM. Black-fly larvae use filtering labial fan covered with mucus to flocculate DOM out of solution (Ross and Craig, 1980; Ciborowski et al., 1997). They have been shown to utilize organic carbon less than 0.2 mm in size (Hershey et al., 1996), and are thought to consume organic matter ranging in size from 45 mm to 0.091 mm (Ross and Craig, 1980; Morin et al., 1988; Wotton, 1988; Hershey et al., 1996). Gut content analysis has shown that black flies consume mostly detritus (both fine particulate organic matter (FPOM) and DOC (67%) and bacteria (33%), along with small amounts of algae (<1%; Schro¨der, 1986; Hershey et al., 1996). The objective of this study was to determine how lake pH, DOC concentration, and the proportion of wetlands in each lake’s catchment affect the concentration of Hg in Simulium spp. (Diptera, Simuliidae) in streams in Ontario, Canada. Our hypothesis was that total Hg in the black-fly larvae would be positively correlated with DOC, negatively correlated with pH, and positively correlated with % wetland in catchment.

metamorphic and plutonic silicate bedrock, covered with a thin layer of soil (Devito et al., 1999). The streams are primarily forested second or third growth forests. There is some cottage development in the area (Dillon et al., 1994), and no point source for Hg pollution. The region has been affected by acid deposition (particularly Plastic Lake catchment; Dillon et al., 1987); however the region is in slow recovery (Dillon and Evans, 2001; Dillon et al., 2003). The lakes and streams are described in more detail in Dillon et al. (1991) and Molot and Dillon (1993).

2.2. Black-fly collection Collection took place from 26 May through 6 June, 2003 and 2e4 June, 2004. In both 2003 and 2004 black-fly larvae were collected by hand by gathering submerged cobbles to which they were attached. A small subset of sites was analyzed in 2003. These sites were chosen due to their range of pH and DOC concentrations, and are likely to be representative of all streams in this region. Different species with different morphologies will select distinct habitats within the stream, and often a riffle will contain only one species (Lacoursie`re and Craig, 1993; McCreadie and Colbo, 1993; Zhang and Malmqvist, 1996); therefore, most of the black flies are likely to be one species since sampling was confined to one substrate. In 2004 adults were captured as they swarmed around people on the stream bank. The black flies were transported to the nearby Dorset Environmental Science Center using plastic buckets containing native stream water. Because no Hg free water was available, the black flies were not allowed to clear their guts before analysis. Larvae were sorted and identified to genus based on Wood et al. (1963) and Merritt and Cummins (1996). Only individuals from genus Simulium (Diptera: Simuliidae) were used in this analysis. Individuals parasitized by nematodes (as shown by a white swollen abdomen) were not included in analysis. Adults were not identified beyond the level of family. Adult females who had obviously recently fed (as observed by a red swollen abdomen) were not included.

2. Experimental design and methods

2.3. Mercury analysis

2.1. Study site

All insects were stored in 10 mL glass vials and frozen until analysis. At that time, they were dried for 12 h at 40
C in an Isotemp oven (Fisher Scientific), and analyzed for total Hg using a Leco Atomic Mercury Analyzer (AMA, 254). This instrument is a single wavelength atomic absorption

Sampling took place in 17 streams in the District of Muskoka and Haliburton County, Ontario (Fig. 1). The catchments are underlain by Precambrian

Fig. 1. Location of the seven study lakes. Streams chosen for this study are inflows and outflows of these lakes.

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spectrometer. Due to the low amount of Hg in each individual, samples were pooled into three groups of 20 individuals for each stream. No sample analyzed contained concentrations of Hg less than the detection limit (7 ng/g, based on 3 standard deviation of the blanks).

regime the wetland size may have changed in later years. The other streams have not been surveyed in the field; spatial information relating to physiography and land use (including wetland area) is available based on GIS methods and 1:10,000 Ontario base maps.

2.4. Methylmercury analysis

2.6. Statistics

Black flies collected at 6 of the 8 sites in 2004 were analyzed for MeHg. The samples from Dickie outflow and Plastic 1 were not analyzed for MeHg. After being spiked with a known concentration of 201 methyl Hg, a weighed volume of bugs were acid digested using 5 mL of 25% HNO3. A 1-mL aliquot was ethylated using sodium tetraethyl borate (NaBEt4). The volatile ethylated mercury species were collected through bubbling with N2 gas onto a Tenax adsorption trap. After thermal release from the tenax trap, the three types (dimethyl, ethyl, inorganic) of mercury compounds were separated using a chromosorb W column. The individual Hg isotopes in the methyl Hg peak were analyzed by a Micromass Platform ICP-MS (hexapole) to calculate isotope ratios, total concentration and percent recovery. This method was modified from (Hintelmann and Evans, 1997; Hintelmann and Ogrinc, 2003).

The data were tested for normality using a ShapiroeWilks test (SPSS version 9.0). Wetland area, the only factor not normally distributed, was log transformed to achieve a normal distribution. Pearson’s correlation was used to evaluate the correlations between variables (SPSS version 9.0). A paired t-test and Levene’s Test of Equality of Error Variances were performed to determine difference in Hg concentration in black flies from 2003 and 2004. Correlations between each variable were also tested for multicolinearity.

2.5. Water analysis In this study we analyzed DOC and pH in each water sample (see Table 1). Water samples were collected using both PET jars and opaque brown Nalgene bottles with a gas cap (for more details see Locke and Scott, 1986). Analyses of Brandy Lake (one stream) and Fawn Lake streams (three streams) were performed at Trent University. These stream samples were analyzed for DOC with a Shimadzu, TOC-Vcpn Total Organic Carbon Analyzer. pH was measured with a Mantech PC titrator plus. The remaining 13 streams were part of the Ontario Ministry of Environment routine sampling program, and were sampled on a weekly (Dickie, Harp and Plastic Lakes) or bi-weekly (Chub and Red Chalk Lakes) basis. The water sample closest to the 30th of May was used in our analysis. Analytical methods and quality assurance protocols used are documented in the Ontario Ministry of the Environment Analytical Methods/Quality Assurance Manual (Teresi, 2003). The pH was measured using an Autoburette titrator (ABU 91), and colorimetry was used to determine dissolved organic carbon concentration in water (Technicon Autoanalyzer II SC Colorimeter). The data for wetland area with in a catchment originated from two sources. Plastic Lake and Red Chalk Lake sub-catchments were surveyed in the field using a level and transit in 1979 (Girard et al., 1985). The wetland areas are thus very accurate for that year; however, due to yearly changes in water

Brandy Lake inflow Chub Lake inflow #1 Chub Lake outflow Dickie Lake inflow #6 Dickie Lake inflow #8 Dickie Lake outflow Fawn Inflow #1 Fawn Inflow #2 Fawn Outflow Harp Lake inflow #3 Harp Lake inflow #4 Harp Lake outflow Plastic Lake inflow Plastic Lake outflow Red Chalk Lake inflow #1 Red Chalk Lake inflow #2 Red Chalk Lake outflow

21 25 3 44 74 3 27 8 21 9 34 5 7 5 13 22 7

2003 27.5 8.5 5.7 19.8 21.7 5.4 28.7 4.4 10.9 14 4.9 3.9 16.4 2.5 5.5 15.8 2.9

2004

19.7 18.9 6

12.2 6.1 5 12.4 2.4

½mg=g Hg WW ¼ ½mg=g Hg DWð1  ð%moisture=100ÞÞ: ð1Þ

pH 2003 2004 6.55 5.49 5.91 4.53 5.02 6.19 4.36 6.36 6.32 5.85 6.41 6.66 4.51 5.61 5.79 4.44 6.64

0.70 1st inflow 2nd inflow outflow

0.60

4.76 4.64 6.21

5.88 6.44 6.71 4.37 4.4

Hg µg/g DW

Wetland area % DOC (mg/L)

The concentration of total Hg (THg) in Simulium spp. larvae ranged from 0.06 to 0.64 mg Hg/g dry weight (DW; Figs. 2 and 3), and adult Hg concentration ranged from 0.15 to 0.75 mg Hg/g DW (Fig. 4). The concentration of MeHg ranged across the sites from 0.087 to 0.309 mg/g; additionally, the proportion of THg that is MeHg ranged from 58% to 93% (Fig. 3). In most of the sites, the THg concentration did not significantly change from 2003 to 2004. The exceptions are the streams around Dickie lake, which are significantly (Dickie inflow 6 p < 0.001, Dickie inflow 8 and Dickie outflow p < 0.05) lower in 2004 than 2003 (Figs. 2 and 3). The variation in THg concentration of the black-fly larvae was significantly greater (Levene stat. ¼ 5.47, p ¼ 0.024), and showed greater variation around the regression line (Figs. 5 and 6) in the inflows than the outflows. By using average moisture content (92  3.0%), conversion from Hg concentration on a DW basis to wet weight (WW) basis can be performed using the calculation below:

For example, the black-fly larvae with the highest Hg concentration (Dickie inflow 6 2003), had Hg concentrations of 0.64 mg/g DW, which is equivalent to 0.050 mg/g WW or 50 ng/g WW.

Table 1 Average water chemistry parameters for each stream Site

3. Results

0.50 0.40 0.30 0.20 0.10 0.00 Brandy

Chub

Dickie

Fawn

Harp

Plastic

Red Chalk

Fig. 2. Average total Hg concentrations in mg/g dry weight (DW) in larval black flies from the inflows and outflows of seven lakes in 2003. The bars represent one standard deviation.

K.M. Harding et al. / Environmental Pollution 143 (2006) 529e535

532 0.45 93.0%

0.35

Hg µg/g DW

THg MeHg

80.2% 88.9%

0.30 58.2%

0.25 0.20

72.1%

0.15

0.70

66.9%

0.60

Hg µg/g DW

0.40

0.10

0.50 0.40 0.30 0.20 0.10

0.05

0.00

0.00 Dickie 6

Dickie Dickie Harp 3 Harp 4 8 out

Harp out

0

Plastic Plastic 1 out

4. Discussion Most organisms obtain Hg directly from their food source (Jackson, 1991; Spry and Wiener, 1991; Mason et al., 2000); therefore, predatory insect species are expected to have higher MeHg and Hg body burdens than species at lower trophic levels. Collector-gatherer and shredder-detritivore insects from natural lakes in Ontario and Quebec range in total Hg from 0.05 to 0.2 mg/g DW, while predatory insects from the same lakes can be as high as 0.4 mg/g DW (Tremblay and Lucotte, 1997; Wong et al., 1997; Tremblay et al., 1998). The black-fly larvae in this study have a range of total Hg body burden similar to that of predatory insects, although they are at the bottom of the food web. The only other study

10

15

20

25

30

y = 0.011x + 0.13

DOC mg/L

r2 = 0.66 p<0.001

Fig. 3. Average Hg and MeHg concentration in mg/g dry weight (DW) in larval black flies from eight streams in 2004. The samples for Plastic 1 and Dickie out were not analyzed for MeHg. The bars represent one standard deviation. Number above the bars represents the percentage of total Hg that is MeHg.

0.70 inflow outflow

0.60

Hg µg/g DW

For these study sites, % wetland in the stream catchment was strongly correlated with DOC concentration (rs ¼ 0.72, p < 0.001), and pH and DOC also correlated strongly (rs ¼ 0.79, p < 0.001) together. This means that the effect of pH, DOC and wetland area on Hg bioaccumulation can not be determined alone. The black-fly larvae had total Hg concentration that was correlated with both DOC (r2 ¼ 0.66, p < 0.001; Fig. 5) and % wetland (r2 ¼ 0.54, p ¼ 0.005; Fig. 6). There was also a strongly significant (r2 ¼ 0.69, p < 0.001) relationship between pH and Hg concentration in Simulium spp. larvae (Fig. 5).

5

0.50 0.40 0.30 0.20 0.10 0.00 4.0

4.5

5.0

5.5

6.0

6.5

7.0

y = -0.10x + 0.82

pH

r2 = -0.69 p<0.001

Fig. 5. Influence of DOC and pH on Hg bioaccumulation in larval Simulium spp.

examining Hg concentration in black-fly larva was located downstream from a chlor-alkali plant in Tennessee; there, the total Hg concentration in Simulium vittatum was 0.07  0.036 mg/g WW (Lindsay and Dimmick, 1983). The black-fly larvae from this polluted Tennessee stream had comparable Hg body burdens to the site with highest Hg body burdens in Ontario. Herbivorous insect species have between 15% and 50% of their total Hg in the form of MeHg (Mason et al., 2000), while in predatory species, such as dragonflies, MeHg ranges from 68% to 95% of the total Hg (Mason et al., 2000; Haines et al., 2003). Black flies have MeHg proportions similar to predatory insects (from 58% to 93%). Black-fly larvae are 0.70

0.60 0.50 0.40

Hg µg/g DW

1st inflow 2nd inflow outflow

0.70

Hg µg/g DW

inflow outflow

0.60

0.80

0.50 0.40 0.30 0.20

0.30

0.10

0.20

0.00 0

0.10

20

40

% wetland

60

80 y = 0.16x + 0.074 2 r = 0.54 p=0.005

0.00 Dickie

Harp

Plastic

Fig. 4. Average Hg concentration in mg/g dry weight (DW) in adult black flies from eight streams in 2004. The bars represent one standard deviation.

Fig. 6. Correlation between log (% wetland) and Hg concentration in larval Simulium spp. Data from Dorset Environmental Science Center (DESC) data base and Rapid Assessment Technique (RAT) data base.

K.M. Harding et al. / Environmental Pollution 143 (2006) 529e535

unusual among stream organisms (Wotton, 1990; Merritt and Cummins, 1996) in that they feed on DOM (Ross and Craig, 1980; Morin et al., 1988; Wotton, 1988; Hershey et al., 1996). This may be why their MeHg body burden is high compared with other detritivorous organisms. Wetlands (including conifer swamps, peat bogs, and beaver ponds) are a major source of DOC to streams (Dillon and Molot, 1997a,b), which is consistent with the fact that we observed a correlation between % wetland and DOC observed in this study. Wetlands are also a major site for Hg methylation; Hg and MeHg concentration increases downstream of wetlands (Grigal, 2002; Galloway and Branfireun, 2004). This will lead to an increase in MeHg downstream of wetlands, and suggests that black-fly larvae could have a higher concentration of MeHg in sites that have a high percentage of wetlands. In order to determine if this is true, more research is needed on the concentration of MeHg in both streams and in black-fly larvae. Several other studies have found positive correlations between DOC concentration in water and Hg body burden in fish (McMurty et al., 1989; Driscoll et al., 1995). Black-fly larvae are unique in their food gathering methods, and are known to utilize DOC as a food source. The caddis fly, Hydropsyche morosa (Trichoptera, Hydropsychidae), has lower total Hg concentration when consuming algae and detritus, and higher Hg concentration when consuming detritus alone (Snyder and Hendricks, 1995). Since black-fly larvae are consuming detritus, fine particulate organic matter and DOC, their Hg body burden is higher than would be expected from low trophic level organisms. By consuming Hg and MeHg bound to DOC, black-fly larvae represent one entry point for MeHg into the food web. There was higher variation in Hg concentration observed in black-fly adults compared with larvae, probably due to the fact that adult samples included a combination of genera. Unlike the larvae, where samples collected from a small section of stream are likely to contain a single species, the adult samples almost certainly represent a mix of species. Furthermore, we did not separate gravid females, and could have included some females with a small blood meal, both of which will induce variation in Hg levels. The high acidity of several sites in this region is unlikely to have a direct toxic effect on Simulium spp, since they are fairly acid tolerant (Chmielewski and Hall, 1993); however, acidification does affect Hg bioaccumulation. Fluctuations in pH influence the amount of Hg bound to DOC (Hintelmann et al., 1997; Drexel et al., 2002). When water pH drops Hg methylation increases (Gilmour and Henry, 1991), which increases the amount of biologically available Hg. The increase in Hg concentrations in acidic conditions in blackfly larvae is probably due to a combination of both of these factors. High acidity is correlated with elevated Hg and MeHg concentrations in fish (McMurty et al., 1989; Wren et al., 1991; Driscoll et al., 1995) and zooplankton (Westcott and Kalff, 1996). However, acidification effects on Hg bioaccumulation in insects are poorly understood (Wren and Stephenson, 1991).

533

Simuliidae larvae are a significant food source to fish, and can comprise 70e80% of stomach content of brook trout Salvelinus fontinalis (Allan, 1981), and 50e90% of stomach content in Arctic grayling, Thymallus arcticus (Jones et al., 2003). If such a high proportion of fish diet is black-fly larvae (with concentrations of MeHg ranging from 0.087e0.309 mg/g), this could be a significant source of MeHg to fish, and should not be overlooked. The high level of Hg in adult Simuliidae suggests that there is movement of Hg out of stream ecosystems and into terrestrial systems. Consumption of adult Diptera (including Simuliidae) can influence mercury concentration in tree swallows, Tachycineta bicolor (Gerrard and St Louis, 2001) and wood ducks, Aix sponsa (Lindsay and Dimmick, 1983). More research is needed to determine the concentration of MeHg present in these black flies and the transfer of Hg and MeHg from black flies to other organisms. 5. Conclusion In this region, the concentration of total Hg and the percentage MeHg in black-fly larvae is elevated above that found for other collector-gatherer and shredder-detritivore insects. These streams are characterized as having acidic conditions and high concentrations of DOC. The concentration of total Hg in the black-fly larvae is correlated with both DOC and pH. This means that in areas downstream from wetlands (a major source of DOC and MeHg), and in regions impacted by acid deposition, black-fly larvae are likely to have high concentrations of total Hg. Their unique feeding habits allow them to consume Hg and MeHg directly from the water column as DOC-Hg complexes. Since black flies are significant food for fish and birds, they represent an important entry point for Hg and MeHg into the food web. Acknowledgements Thanks to Keith Somers, Ron Reid, Joe Findes and Chris Jones of the Dorset Environmental Science Center for their help picking sites and for water chemistry analysis. Many thanks to Denina Simmons, Magda Havas, Doug Evans, and Eavan O’Connor for their help editing this document. Thanks should also go to Heather Broadbent, Katya Epova, and Joy Zhu for assistance in MeHg analysis. References Allan, J.D., 1981. Determinants of diet of brook trout (Salvelinus fontinalis) in a mountain stream. Canadian Journal of Fisheries and Aquatic Sciences 38, 184e192. AMAP, 1998. AMAP Assessment Report: Arctic Pollution Issues. Arctic Monitoring and Assessment Programme (AMAP), Olso, Norway. Chmielewski, C.M., Hall, R.J., 1993. Changes in the emergence of blackflies (Diptera: Simuliidae) over 50 years from Algonquin Park streams: is acidification the cause? Canadian Journal of Fisheries and Aquatic Sciences 50, 1517e1529. Ciborowski, J.J.H., Craig, D.A., Fry, K.M., 1997. Dissolved organic matter as food for black fly larvae (Diptera: Simuliidae). Journal of the North American Benthological Society 16, 771e780.

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