Polar Biol (2014) 37:1785–1796 DOI 10.1007/s00300-014-1561-3
ORIGINAL PAPER
Ecological determinants of methylmercury bioaccumulation in benthic invertebrates of polar desert lakes John Che´telat • Alexandre J. Poulain • Marc Amyot • Louise Cloutier • Holger Hintelmann
Received: 22 January 2014 / Revised: 13 August 2014 / Accepted: 21 August 2014 / Published online: 21 September 2014 Ó @Her Majesty the Queen in right of Canada 2014
Abstract We investigated concentrations of monomethylmercury (MMHg) at the base of benthic food webs in six lakes from polar desert (biologically poor and low annual precipitation) on Cornwallis Island (Nunavut, Canada, *75°N latitude). Anthropogenic mercury emissions reach the Arctic by long-range atmospheric transport, and information is lacking on processes controlling MMHg entry into these simple lake food webs, despite their importance in determining transfer to lake-dwelling Arctic char. We examined the influences of diet (using carbon and nitrogen stable isotopes), water depth, and taxonomic composition on MMHg bioaccumulation in benthic invertebrates (Chironomidae and Trichoptera). We also estimated MMHg biomagnification between benthic algae and invertebrates. Similar MMHg concentrations of chironomid larvae in
J. Che´telat (&) National Wildlife Research Centre, Environment Canada, Ottawa, ON K1A 0H3, Canada e-mail:
[email protected] A. J. Poulain Department of Biology, University of Ottawa, Ottawa, ON, Canada M. Amyot Groupe de recherche interuniversitaire en limnologie, and Centre d’e´tudes nordiques, De´partement de sciences biologiques, Universite´ de Montre´al, Montre´al, QC, Canada L. Cloutier Collection entomologique Ouellet-Robert, De´partement de sciences biologiques, Universite´ de Montre´al, Montreal, QC H3C 3J7, Canada H. Hintelmann Environmental Resource Studies Program, Department of Chemistry, Trent University, Peterborough, ON, Canada
nearshore and offshore zones suggest that benthic MMHg exposure was homogeneous within the lakes. Chironomid d13C values were also similar in both depth zones, suggesting that diet items with highly negative d13C, specifically methanogenic bacteria and planktonic organic matter, were not important food (and therefore mercury) sources for profundal larvae. MMHg concentrations were significantly different among two subfamilies of chironomids (Diamesinae, Chironominae) and Trichoptera. Higher MMHg concentrations in Diamesinae were likely related to predation on other chironomids. We found high MMHg biomagnification between benthic algae and chironomid larvae compared with literature estimates for aquatic ecosystems at lower latitudes; thus, benthic processes may affect the sensitivity of polar desert lakes to mercury. Information on benthic MMHg exposure is important for evaluating and tracking impacts of atmospheric mercury deposition and environmental change in this remote High Arctic environment. Keywords Polar desert Chironomids Methylmercury Carbon stable isotopes Biomagnification
Introduction Mercury is a contaminant of concern due to its long-range atmospheric transport to the Arctic and high levels found in some traditional food species consumed by northerners (AMAP 2011; NCP 2012). Most mercury in the environment is in an inorganic form, whereas organic monomethylmercury (MMHg) is the more toxic species that biomagnifies through food webs. Elevated exposure to MMHg has the potential for toxicological effects on Arctic biota (Dietz et al. 2013) and the northerners that consume them (Donaldson et al. 2010; Tian et al. 2011). Long-term
123
1786
environmental monitoring in the Canadian Arctic indicates that mercury concentrations have been increasing in some animal populations in recent decades (NCP 2012). Information is currently lacking on the processes controlling concentrations of MMHg at the base of food webs in Arctic fresh waters, despite their importance in determining MMHg transfer to fish. Much of the Canadian Arctic Archipelago is polar desert, characterized by low biological diversity, little terrestrial plant cover, and low annual precipitation of less than 150 mm (Callaghan et al. 2005). Lakes in polar desert have an impoverished number of aquatic species and contain simple food webs essentially consisting of Arctic char (Salvelinus alpinus), chironomids (Diptera, Chironomidae) and basal resources with only a few other invertebrate species occurring at low densities, including one species of Trichoptera (Hobson and Welch 1995). Chironomids are the main pathway for MMHg transfer to landlocked Arctic char because of their importance as prey (Gantner et al. 2010b). These insects likely also accumulate most of their MMHg through their diet (Tsui and Wang 2004), which consists primarily of algae and detritus on surfaces of sediment and rocks (Che´telat et al. 2010). Chironomids, particularly the larvae, are a useful indicator of MMHg uptake in food webs of polar desert lakes because of their trophic importance and their association with specific benthic habitats within a lake. Adult chironomids are consumed less by Arctic char because they can only be preyed on as they emerge from the lake water in summer (Gallagher and Dick 2010). Chironomids have four main developmental stages in their life cycle and undergo complete metamorphosis. Fertilized eggs are deposited on the water surface and sink to the lake bottom where they hatch as larvae within a month (Welch 1976). In the High Arctic, larvae typically inhabit benthic environments for 2–3 years before reaching maturity (Welch 1976). At the end of their life cycle in spring or summer, the larvae develop wing pads, molt to pupae (an inactive period when adult structures are formed), and then swim to the water surface where the adults shed their skin to emerge. Mating occurs in the air or on ice or terrestrial substrates following emergence. Previous research on High Arctic chironomids identified metamorphosis as a key biological process that concentrated MMHg in adults by up to three times relative to immature stages (Che´telat et al. 2008). Environmental characteristics (specifically drainage basin size, mercury levels in water and sediment, water temperature, and dissolved organic carbon) also explained a small portion of differences in chironomid MMHg concentrations among High Arctic lakes and ponds (Che´telat et al. 2008). The influence of ecological factors such as habitat preference, diet and taxonomy on the bioaccumulation of MMHg in High Arctic chironomids has received little study. This may in part be due to challenges in collecting
123
Polar Biol (2014) 37:1785–1796
small-sized larvae from benthic substrates in sufficient quantities for mercury analysis. Carbon and nitrogen stable isotopes are powerful ecological tracers that provide information on dietary sources or the trophic position of organisms, respectively (Fry 2006). A recent investigation (using carbon and nitrogen stable isotopes) showed striking interspecies variation in the diet of Arctic chironomids from Greenland lakes (Reuss et al. 2013). At lower latitudes, delta values of carbon stable isotopes in larval chironomids are often more negative in offshore, deeper waters relative to the shoreline (Vander Zanden and Rasmussen 1999; Hershey et al. 2006; Syva¨ranta et al. 2006; Jones et al. 2008). These patterns have been related to a different diet in profundal zones, shifting from littoral benthic algae to the consumption of methanogenic bacteria (Jones et al. 2008) or phytoplankton biomass that has settled from the water column (Doi et al. 2006; Premke et al. 2010). For polar desert lakes, we hypothesized that the MMHg concentrations of chironomid larvae may be influenced by water depth preference due to variation in diet (i.e., littoral benthic algae vs. phytoplankton and methanogenic bacteria) or to differences in MMHg exposure. Sediment methylation rates may be depth-dependent in lakes (e.g., higher in profundal than shallow zones), which could result in habitat variation in food web uptake. Nearshore substrates are often rocky in polar desert lakes lacking the finer sediments (more conducive for methylation) found in deeper water. In contrast, snowmelt loadings of MMHg to lakes during spring (Loseto et al. 2004) could potentially impact nearshore benthic invertebrates more than those in deeper water. Taxonomic variation in feeding (e.g., collector-gatherer versus predator) may also play a role in MMHg bioaccumulation. The influences of diet, water depth and taxonomic composition on MMHg bioaccumulation in benthic food webs have not been previously investigated in polar desert lakes. Polar desert lakes on Cornwallis Island (*75°N latitude, in Nunavut, Canada) have been the focus of considerable research on mercury cycling over the last two decades (Amyot et al. 1997; Loseto et al. 2004; Muir et al. 2005; Che´telat et al. 2008; Gantner et al. 2010b), and several lakes are monitored for temporal mercury trends under the Northern Contaminants Program of the Government of Canada (NCP 2012). The overall objective of this study was to examine the influence of ecological factors on MMHg bioaccumulation in benthic invertebrates from those lakes. We focused on MMHg because it is the more toxic form and biomagnifies in food webs, in contrast to inorganic mercury. The specific goals were to: (1) determine whether MMHg bioaccumulation in chironomids differs between nearshore and offshore zones; (2) examine the influence of diet on MMHg bioaccumulation using carbon and nitrogen stable isotopes; (3) determine the extent of taxonomic variation in MMHg
Polar Biol (2014) 37:1785–1796
1787
Table 1 Location and physical characteristics of six polar desert lakes on Cornwallis Island, Nunavut, Canada, 2011 Lake
Latitude (°N)
Longitude (°W)
Lake surface area (km2)
Watershed area (km2)
Amituk
75°020 44
93°470 15
Maximum depth (m)
0.38
26.50
Char
74°42 16
94°520 56
0.53
3.47
27.5
Meretta
74°410 36
94°590 38
0.26
8.71
12 14
0
0
0
43
Plateau
74°48 36
95°12 00
0.70
6.33
Resolute
74°410 31
94°560 44
1.18
17.03
22
Small
74°450 37
95°030 35
0.14
1.50
11
North Latitude
West Longitude Ellesmere Island Amituk Plateau
Small
Meretta Char
Resolute
Resolute Bay
Cornwallis Island
Victoria Island
Baffin Island
Fig. 1 Geographic locations of the six polar desert lakes studied on Cornwallis Island, Nunavut, Canada, 2011. Note the distance scale (km) is for the larger map of islands in the Arctic Archipelago
123
1788
bioaccumulation in benthic invertebrates; and (4) estimate the biomagnification of MMHg between benthic algae and chironomids.
Materials and methods Field sampling Six lakes were sampled near the community of Resolute Bay on Cornwallis Island (Nunavut) in August of 2011 (Table 1; Fig. 1). The region has a polar desert climate characterized by cold temperatures (February daily average = -33 °C, July daily average = 4 °C), low annual precipitation (150 mm), and a short ice-free season for lakes that lasts approximately 2 months. Water temperatures remain cold throughout the ice-free season (generally below 10 °C) and persistent thermal stratification does not occur. The study lakes vary in their size and water depth (Table 1) but have similar water chemistry characterized by an alkaline pH (*8) and very low concentrations of dissolved organic carbon (\2 mg L-1), total phosphorus (\5 lg L-1), chlorophyll a (\2 lg L-1), total mercury (\1.5 ng L-1), and MMHg (B0.05 n L-1) (Che´telat et al. 2008; Gantner et al. 2010b). Meretta Lake received untreated sewage from the local airport between 1949 and 1998, although the greatest inputs occurred in the earlier decades of that time period. The water quality of the lake has since returned to near baseline conditions (Antoniades et al. 2011). Chironomid larvae were collected from shallow nearshore areas (\1.25 m deep) with a D-framed kicknet of 500 lm mesh and from sediment in offshore, deeper waters (3–30 m depth) with an Ekman grab. Sediment was removed from grabs with a 500-lm-mesh sieve. Typically, three nearshore and three offshore stations were sampled in each lake although additional stations were occasionally sampled (e.g., seven offshore stations in Amituk Lake). A small inflow stream to Char Lake, which receives snowmelt water for much of the summer (identified as inflow #3 in Schindler et al. (1974)), was also sampled for chironomid larvae with a kicknet. In a few cases, an insufficient sample of larvae was obtained from some lake stations. Larvae samples were placed in ziplock bags with ambient water and brought back to the laboratory for processing within 6–12 h on the same day of collection. The approximate time for gut clearance of chironomids is 24 h (Grey et al. 2004), and therefore, the larvae likely contained gut contents. In the laboratory, chironomid larvae were removed from sediment material with tweezers, washed in ultrapure water, placed in acid-cleaned plastic vials and frozen until analysis. Larvae collected from different stations within a lake were treated as separate
123
Polar Biol (2014) 37:1785–1796
replicates. For most samples, no separation of chironomid taxa was conducted. However, when sufficient amounts of larvae were available, individuals were separated by subfamily (i.e., Diamesinae, Chironominae) and placed in separate vials for analysis (N = 1–3 per taxon per lake). A few larvae from each subfamily were also preserved in 70 % ethanol for verification of identifications by Louise Cloutier (coordinator of the Ouellet-Robert Entomological Collection, Universite´ de Montre´al). Chironomid larvae in the samples were primarily third or fourth instars. One species of Trichoptera (Apatania zonella) was found at nearshore stations in most lakes and was sampled and processed in the same manner for the purpose of comparison to chironomids. The larva of this Trichopteran species is a scraper and likely consumes benthic algae and detritus, similar to chironomids in the lakes (Jorgenson et al. 1992; Hobson and Welch 1995). Caddisfly casings were removed on the day of collection and before freezing the samples. Putative resources of benthic invertebrates (benthic algae and organic matter from sediment or nearshore rock biofilms) were sampled to measure MMHg concentrations in primary producers and stable isotope ratios of basal resources. Macroscopic Nostoc spheres (a genus of cyanobacterial algae) were removed with tweezers from kicknet and Ekman grab material. When present at nearshore stations, filamentous algae were scraped off small rocks into ziplock bags with a nylon-bristle brush. In a few cases, filamentous algae were also collected with tweezers from the surface of offshore Ekman grabs. Fragments of rock biofilms (mats composed of detritus, algae and other microorganisms) were removed from kicknet material with tweezers. The surface layer of offshore sediment (top 1 cm) was sampled from Ekman grabs with a plastic spoon. The macroscopic samples (Nostoc, filamentous algae) were washed with ultrapure water. Putative organic matter resources were placed in 20-mL plastic vials and frozen until analysis. Laboratory analyses Samples of chironomid larvae (N = 56), caddisfly larvae (N = 7) and benthic algae (Nostoc N = 9, filamentous algae N = 9) were analyzed for MMHg concentration (ng g-1 dry wt) according to the method of Cai et al. (1997). Freeze-dried and homogenized samples of invertebrates (1–10 mg) and benthic algae (30–50 mg) were pretreated with an alkaline digestion in KOH followed by acidic digestion in KBr and CuSO4. Bromide derivative of MMHg was extracted in dichloromethane, isolated with sodium thiosulfate and back extracted in dichloromethane for determination by capillary gas chromatography coupled with atomic fluorescence spectrometry. Duplicate blanks and certified reference materials were analyzed with each
Polar Biol (2014) 37:1785–1796
batch of 24 samples. MMHg recoveries were 95 ± 8 % (N = 8) from fish protein homogenate (DORM-3, National Research Council of Canada) and 101 ± 13 % (N = 4) from lobster hepatopancreas (TORT-2, National Research Council of Canada). The analytical detection limit for MMHg was 3 ng g-1 for a 5 mg invertebrate sample and 0.4 ng g-1 for a 40 mg algal sample. Half the detection limit was used for two algal samples with MMHg concentrations below detection. The relative standard deviation of analytical duplicates averaged 8 % (N = 6). All concentrations are presented on a dry weight (wt) basis. Samples of invertebrates (N = 48), filamentous algae (N = 9), nearshore biofilm organic matter (N = 17) and offshore sediment organic matter (N = 19) were analyzed for carbon and nitrogen stable isotope ratios at the G.G. Hatch Stable Isotope Laboratory (University of Ottawa, Ottawa, Canada) on a Thermo Finnigan DeltaPlus XP Isotope Ratio Mass Spectrometer. The ratios are expressed in delta notation (d) as parts per thousand (%) deviation from atmospheric N2 gas standard for nitrogen and Pee Dee Belemnite for carbon. Internal standards (Nicotinamide, ammonium sulfate ? sucrose, caffeine, glutamic acid) were analyzed every 15 samples. Analytical precision based on an internal standard (not used for calibration) was\0.2 % for both d15N and d13C. A blank tin capsule was analyzed with each daily run. Carbon stable isotope measurements for basal resources were not included because of highly enriched stable isotope ratios, likely resulting from inorganic carbon (as carbonate) in the samples. Data analysis Categorical differences among lakes, between nearshore and offshore zones, and among invertebrate taxa were tested with t tests and one-way ANOVAs. Amituk Lake was excluded from the test for differences in chironomid MMHg concentrations between nearshore versus offshore zones because of insufficient samples from the nearshore zone. In that lake, nearshore larvae were difficult to collect (despite repeated effort) because of steep, rocky slopes. Pearson’s correlations were calculated to examine associations between MMHg concentrations and stable isotopes of carbon and nitrogen in chironomids. Variables were log-transformed to achieve normality and homoscedasticity. When these conditions could not be achieved or within-group sample sizes were low (N = 2–3), then equivalent nonparametric tests were used (Mann–Whitney rank-sum test, Kruskal–Wallis). Probability values of post hoc comparisons for one-way ANOVAs were Holm-corrected for the experiment-wise error rate. Means are presented with ±1 standard error, unless indicated. Geometric means are presented for one-way ANOVA results (if the independent variable was log-transformed). Biomagnification factors were calculated as the ratio of MMHg concentration in invertebrates over the MMHg concentration in benthic algae.
1789
Fig. 2 Mean log MMHg concentrations (±1 standard error) in chironomid larvae from six polar desert lakes on Cornwallis Island, Nunavut, Canada, 2011. Letters identify significant differences between lakes (one-way ANOVA, Holm P \ 0.05). Sample sizes are at the base of the bars
Results Among- and within-lake differences in chironomid MMHg concentrations The study lakes had similar average log MMHg concentrations in larval chironomids, except for Amituk where levels were three to four times higher than in the other lakes (Fig. 2; one-way ANOVA: P \ 0.001, N = 36, Holm P B 0.001 for pair-wise comparisons between Amituk and other lakes). MMHg concentrations of chironomid larvae in the other five lakes were relatively low with geometric means ranging from 30–41 ng g-1 (Fig. 2). These minor differences were not significant (Holm P C 0.978 for pair-wise comparisons). No effect of water depth was found in a comparison of chironomid log MMHg concentration between the shallow nearshore zone (36 ± 5 ng g-1, N = 14) and deeper offshore zone (33 ± 5 ng g-1, N = 14) when data were pooled across lakes (t test, P = 0.662). Amituk Lake was excluded from this analysis due to insufficient samples from the nearshore zone and elevated MMHg concentrations relative to the other lakes. The pattern was consistent within each lake, where MMHg concentrations overlapped between zones, albeit to a lesser extent in Plateau Lake (Fig. 3). Additional sampling is warranted for Amituk Lake, where a sample of nearshore chironomids (Table 3) and nearshore Trichoptera (Table 4) had MMHg concentrations that were similar to the other lakes and much lower than the offshore Amituk samples. Overall, these observations show that chironomid MMHg bioaccumulation was similar between nearshore and offshore zones in five polar desert study lakes. Interestingly, chironomid larvae collected from a small stream flowing into Char Lake had a very similar MMHg concentration (37 ng g-1) to chironomids in nearshore and
123
1790
Polar Biol (2014) 37:1785–1796
Fig. 3 A comparison of log MMHg concentrations in individual samples of chironomid larvae from nearshore and offshore zones in five of the polar desert lakes on Cornwallis Island, Nunavut, Canada, 2011. Insufficient nearshore data were available to include Amituk Lake
offshore zones of that lake, highlighting the lack of spatial variability in the system (Table 2). Depth variation in chironomid feeding using carbon and nitrogen stable isotopes Across lakes, mean d13C values of chironomid larvae were not significantly different between the nearshore zone (-23.8 ± 0.6 %, N = 17) and offshore zone (-24.6 ± 0.5 %, N = 26) (t test, P = 0.290). Further, there was no correlation between the log depth of collection and d13C values of chironomid larvae (P = 0.886, N = 43; Fig. 4). There was a weak association between the d13C and log MMHg concentration of chironomids (Pearson r = 0.32, P = 0.036, N = 43). However, this correlation was due to elevated MMHg in Amituk chironomids that also had higher d13C values, and it was not significant when this lake was excluded (P = 0.581, N = 36). Together, these
Fig. 4 Variation in d13C values of chironomid larvae with lake depth in six polar desert lakes on Cornwallis Island, Nunavut, Canada, 2011. No correlation was found (Pearson r, P = 0.886, N = 43)
results suggest that water depth did not influence the diet of chironomids, which could explain their comparable MMHg bioaccumulation in nearshore and offshore zones. In contrast, mean d15N values of chironomid larvae were higher in offshore (6.3 ± 0.3 %, N = 26) relative to nearshore samples (4.4 ± 0.4 %, N = 17) (t test, P \ 0.001). This difference was due to more positive d15N values in organic matter sources offshore (Fig. 5). Pooled across lakes, the median d15N of organic matter in offshore sediment (5.0 %) was enriched twofold relative to epilithic biofilms nearshore (2.4 %) (Mann–Whitney rank-sum test, P \ 0.001, N = 36), and this general pattern was observed for all lakes except Small (Fig. 5a). The d15N of putative organic matter sources at sampling sites was positively correlated with the d15N of larval chironomids (Pearson
Table 2 Mean (±1 standard deviation) MMHg concentrations and d13C and d15N values of pooled taxa of chironomid larvae collected in nearshore and offshore zones of six polar desert lakes on Cornwallis Island, Nunavut, Canada, 2011 Lake Amituk Char
Meretta
Zone
N
MMHg (ng g-1)
N
d13C (%)
d15N (%)
Nearshore
1
44
–
–
Offshore
7
184 ± 77
7
-22.2 ± 0.9
5.6 ± 0.3
Nearshore
4
37 ± 8
3
-27.1 ± 1.7
3.4 ± 0.5
1
Offshore
3
36 ± 18
Inflow
2
37 ± 2
-25.7
5.4
–
–
Nearshore
3
57 ± 12
3
-21.2 ± 1.2
4.4 ± 0.1
Offshore
3
31 ± 9
3
-25.8 ± 4.4
5.5 ± 2.1
Plateau
Nearshore
2
17 ± 4
2
-23.2 ± 2.5
3.0 ± 0.1
Offshore
3
57 ± 48
2
-24.4 ± 0.7
5.6 ± 1.0
Resolute
Nearshore
3
41 ± 20
3
-26.1 ± 0.4
5.7 ± 0.8
Offshore
2
29 ± 18
2
-23.9 ± 3.1
8.8 ± 0.8
Small
Nearshore
2
36 ± 4
1
-25.1
2.3
Offshore
3
35 ± 12
3
-25.9 ± 1.4
6.6 ± 1.6
123
Polar Biol (2014) 37:1785–1796
1791
Fig. 6 A taxonomic comparison of mean log MMHg concentrations (±1 standard error) in larvae of two chironomid subfamilies and Trichoptera pooled across five polar desert lakes on Cornwallis Island, Nunavut, Canada, 2011. Letters identify significant differences (one-way ANOVA, Holm P \ 0.05). Sample sizes are at the base of the bars
Fig. 5 a Comparison of d15N values for individual samples of benthic organic matter from nearshore and offshore zones within six polar desert lakes on Cornwallis Island, Nunavut, Canada, 2011. b Relationship between mean d15N values of chironomid larvae and benthic organic matter in nearshore and offshore zones of the six lakes (Pearson r = 0.72, P = 0.013, N = 11). No d15N data were available for nearshore larvae of Amituk Lake
r = 0.72, P = 0.013, N = 11; Fig. 5b). Trophic fractionation of d15N was estimated between putative organic matter sources and chironomid larvae (excluding samples of a potentially predatory taxon), giving a mean fractionation of 1.4 % (±0.3 %, N = 37). After adjusting chironomid d15N values for variation in baseline organic matter signatures (measured in each lake and depth zone), there was no correlation with chironomid log MMHg concentrations, either with Amituk Lake included (P = 0.077, N = 43) or not (P = 0.711, N = 35). This result indicates that trophic variation was not an important determinant of spatial variation in chironomid MMHg bioaccumulation, likely because the chironomids were predominately primary consumers and fed at a similar trophic position. Taxonomic variation in invertebrate MMHg concentrations Using taxon-specific samples (sorted to subfamily for chironomids) from Char, Small, Resolute, Plateau and Meretta
lakes, we found that log MMHg concentration varied among invertebrate taxa (one-way ANOVA, P \ 0.001, N = 18; Fig. 6). Trichoptera (caddisflies) had the lowest MMHg concentrations across the lakes, followed by Chironominae chironomids (commonly referred to as blood worms) and Diamesinae chironomids (Fig. 6). Sufficient sample material of Orthocladiinae chironomids was not available for comparison. The concentrations in Trichoptera and Chironominae generally showed little among-lake variation, while those for Diamesinae showed twofold differences (Table 3). There was no significant difference in adjusted d15N values between the three taxonomic groups (one-way ANOVA, P = 0.075, N = 16). However, there was a positive correlation between invertebrate log MMHg concentration and the adjusted d15N value of individual samples (Pearson r = 0.62, P = 0.010, N = 16), and Diamesinae with the highest MMHg concentrations also had higher d15N. This result suggests that higher MMHg concentrations in Diamesinae chironomids were due to predatory feeding. Biomagnification of MMHg at the base of the food web Benthic algae had MMHg concentrations that ranged from 0.4 to 10.8 ng g-1 (Table 4), and no difference was found between the nearshore zone (geometric mean = 1.5 ± 0.9 ng g-1, N = 8) and offshore zone (geometric mean = 1.8 ± 0.8 ng g-1, N = 8) (t test, log MMHg, P = 0.747). Since chironomid larvae in five of the six lakes did not differ in their MMHg concentration (Fig. 2), a biomagnification factor between benthic algae and chironomid larvae was calculated using the MMHg concentrations averaged over those lakes. Similar to the chironomid larvae, there was not a significant difference in benthic algal MMHg concentration among the five lakes (Kruskal–Wallis
123
1792
Polar Biol (2014) 37:1785–1796
Table 3 Mean (±1 standard deviation) MMHg concentrations and d13C and d15N values of three sorted taxa of benthic invertebrates from nearshore and offshore zones of six polar desert lakes on Cornwallis Island, Nunavut, Canada, 2011
Lake
Taxon
Amituk Char
Meretta
Zone
MMHg (ng g-1)
d13C (%)
d15N (%)
Trichoptera
Nearshore
1
21
–
–
–
Offshore
1
217
–
–
–
Trichoptera
Nearshore
1
22
1
-28.6
3.4
Chironominae
Offshore
1
58
1
-28.1
6.1
Diamesinae
Offshore
1
37
1
-25.8
5.5
Chironominae
Nearshore
1
37
1
-20.4
5.1
Nearshore
1
93
1
-20.4
7.3
Plateau
Trichoptera
Nearshore
1
18
–
–
–
Resolute
Trichoptera
Nearshore
3
22 ± 3
3
-27.9 ± 3.4
5.7 ± 1.2
Chironominae
Offshore
2
28 ± 3
2
-24.2 ± 0.9
8.1 ± 0.6
Diamesinae
Nearshore
1
44
1
-23.7
7.6
Diamesinae
Offshore
2
41 ± 8
2
-25.5 ± 0.1
8.6 ± 0.04
Trichoptera
Nearshore
1
26
1
-26.3
3.6
Chironominae
Offshore
1
27
1
-27.4
3.5
Diamesinae
Offshore
2
87 ± 3
1
-27.3
6.5
N
d13C (%)
d15N (%)
Amituk
2
0.5 ± 0.2
2
-12.1 ± 0.7
1.4 ± 0.02
Char
3
4.0 ± 1.9
2
-28.3 ± 2.2
2.9 ± 0.5
Meretta
3
6.4 ± 5.4
2
-18.3 ± 0.5
2.9 ± 0.2
Plateau
2
0.8 ± 0.3
–
–
–
Resolute
4
4.5 ± 3.7
3
-21.6 ± 3.8
7.2 ± 1.9
Small
4
0.9 ± 0.6
2
-21.7 ± 8.1
5.5 ± 5.0
Note that d15N values for Nostoc spheres were not included because they have distinct signatures due to internal nitrogen fixation
test, P = 0.114, N = 16). Based on among-lake average concentrations (average MMHg ± 95 % CI: benthic algae = 3.4 ± 1.7 ng g-1, N = 16; chironomid larvae = 38.7 ± 7.4 ng g-1, N = 28), MMHg was biomagnified by a factor of 11 between benthic algae and chironomid larvae (95 % CI 6–27). Biomagnification factors for chironomid larvae in individual lakes averaged 23 and ranged from 7–49, although given the low sample sizes for benthic algae in each lake (Table 4), there is greater certainty in our biomagnification estimate based on among-lake average MMHg concentrations. The among-lake biomagnification factor for different invertebrate taxa was 8 for Trichoptera (95 % CI 5–20), 9 for Chironominae (95 % CI 4–25), and 17 for Diamesinae (95 % CI 8–44).
Discussion This study examined the influence of fine-scale ecological factors on MMHg bioaccumulation of benthic invertebrates
123
N
Diamesinae
Table 4 Mean (±1 standard deviation) MMHg concentrations and d13C and d15N values of benthic algae (Nostoc spheres or filamentous forms) in six polar desert lakes on Cornwallis Island, Nunavut, Canada, 2011 N
MMHg (ng g-1)
Diamesinae
Small
Lake
N
in polar desert lakes. We found no influence of water depth on the carbon stable isotopes or MMHg bioaccumulation of chironomids but significant taxonomic differences in benthic invertebrate MMHg concentrations. Further, the biomagnification of MMHg from benthic algae to chironomids was found to be relatively high compared to lower latitude fresh waters. These findings are discussed below in relation to their significance for understanding and tracking the impacts of mercury (including long-range atmospheric transport) to this remote High Arctic environment. Depth variation in chironomid diet and MMHg concentrations Water depth did not influence the dietary carbon sources of chironomid larvae and their bioaccumulation of MMHg. These findings are relevant for two reasons. First, limited diet variation was found, in contrast to lower latitudes lakes, which suggests fewer pathways for uptake and transfer of mercury at the base of the benthic food web of polar desert lakes. Second, the exposure of chironomids to MMHg appeared to be relatively homogenous within these systems. Offshore chironomids in the polar desert lakes did not have more negative d 13C values compared to nearshore zones, and even at depths of 20–30 m in Amituk Lake, d13C values averaged -22 %. In all lakes, average chironomid d13C values were less negative than those for planktonic invertebrates (zooplankton d13C = -33 to -28 %) measured in Che´telat et al. (2012). Highly negative d13C values (i.e., \-35 %) were not observed in larvae from the polar desert lakes, in contrast with lower latitude lakes where values of up to -65 % are measured in profundal chironomids (Jones et al. 2008). Therefore,
Polar Biol (2014) 37:1785–1796
profundal chironomids did not likely consume significant amounts of methanogenic bacteria or settled phytoplankton, which have highly negative d13C values (Vander Zanden and Rasmussen 1999; Jones et al. 2008). While caution is required in interpreting chironomid d13C without having measurements for all organic matter sources, this finding is consistent with a previous isotope mixing model estimate for Small Lake that indicates polar desert chironomids consume primarily benthic algae, which is enriched in 13C (Che´telat et al. 2010). This study builds on the earlier analysis, based primarily on nearshore chironomids, by showing that chironomid d13C values are not more negative in offshore zones. Polar desert lakes have low dissolved organic matter concentrations and highly transparent waters which allow for benthic algal primary production in deep waters (Welch and Kalff 1974). In Char Lake, for example, we found filamentous algal mats on the surface of sediment at 12 and 14 m, indicating sufficient light for growth. Phytoplankton production is limited (Welch and Kalff 1974; Markager et al. 1999), and sedimentation rates of planktonic organic matter are likely very low. In addition, a molecular characterization of the sediment microbial community in one of the study lakes (Char) indicated that methanogenic bacteria are not abundant nor highly active in profundal sediments, which have very low organic matter content (Stoeva et al. 2013). Polar desert lakes are constrained by extreme environmental conditions that limit biological production, and the carbon stable isotopes suggest that pathways of carbon (and mercury) transfer to chironomids via methanogens or planktonic organic matter are not likely important. Similar MMHg concentrations in chironomids from nearshore and offshore zones suggest relatively homogeneous exposure to MMHg within the study lakes. Thermal stratification does not typically occur in these systems due to low water temperatures and prevalent strong winds that promote mixing of the water column (Vincent et al. 2008). Concentrations of total mercury and MMHg in lake water are low and show little within-lake variability (Che´telat et al. 2008). As part of a broader study on mercury cycling, we measured mercury methylation potentials in sediment cores from the study lakes in August of 2010 and 2011 by short-term incubations of mercury stable isotopes using the method of Hintelmann et al. (2000). The measurements suggest that MMHg production in the surface layer of offshore sediments is low (lake averages B0.31 % day-1; H. Hintelmann, unpublished data) relative to values of *1–15 % day-1 in Alaskan lakes (Hammerschmidt et al. 2006) and High Arctic wetlands on Ellesmere Island (Lehnherr et al. 2012). Therefore, the offshore sediments are not high production sites where MMHg exposure would be higher. One exception was Amituk Lake, where we found approximately threefold higher methylation potential in
1793
surface sediment of seven cores (collected at water depths of 6–40 m) as compared to the other lakes. Thus, the elevated MMHg concentrations in Amituk chironomids likely reflect in situ MMHg production in offshore sediment. Amituk Lake is a remote lake, and it has not been disturbed by local human activities. The higher mercury methylation potential in sediments is likely due to lake-specific environmental conditions. Invertebrate taxonomy and baseline d15N values: importance for study designs In this study, we present the first detailed information on taxonomic variation of MMHg bioaccumulation in benthic invertebrates of polar desert lakes. We found differences in MMHg concentrations among two subfamilies of chironomid larvae, with Diamesinae having almost twice the average MMHg of Chironominae. Nitrogen stable isotope ratios indicated that Diamesinae were feeding at a higher trophic position in some lakes but not others. This result builds on earlier observations from chironomid stomach contents that Diamesinae sometimes but not always consume other chironomids as prey (Che´telat et al. 2010) and that higher chironomid MMHg concentrations are correlated with the presence of Diamesinae in taxon-pooled samples (Che´telat et al. 2008). It remains unclear what factors lead to occasional predatory feeding in Diamesinae. Trichoptera larvae had a similar trophic position but lower MMHg concentrations than Chironominae chironomids. These primary consumers may specialize on distinct types of benthic algae or detritus (Grey et al. 2004; Ings et al. 2010; Reuss et al. 2013) that result in differential uptake of MMHg or variation in growth rate could play a role in bioaccumulation (Karimi et al. 2007). Arctic char feed on a variety of chironomid taxa; therefore, taxonomic differences in MMHg concentrations are not likely relevant for overall trophic transfer to fish in polar desert lakes. However, our findings suggest that taxonomic information is relevant when measuring MMHg concentrations in benthic invertebrates because of the potential for sampling biases, particularly from the inclusion of the subfamily Diamesinae. We examined amonglake and within-lake differences in chironomid MMHg concentrations using taxon-pooled samples, and taxonomic composition may have contributed to minor sample variation. Nevertheless, the pooling of taxa did not likely affect our overall conclusions because large Diamesinae larvae were not abundant. Between lake-comparisons of caddisflies and Chironominae, and offshore-nearshore comparisons of Diamesinae within Resolute Lake also showed little variation (Table 3). The taxonomic comparisons involved low sample sizes from each lake (due in part to low biodiversity and logistical challenges) although significant
123
1794
differences were evident when data were pooled across lakes. Further research is warranted to investigate in more detail taxonomic variation in invertebrate MMHg bioaccumulation by including Orthocladiinae chironomids and identifying taxa to a finer resolution. The d15N values of putative organic matter sources varied among lakes and between depth zones within the lakes. It is well recognized that the d15N values of basal resources can vary widely in aquatic ecosystems (Vander Zanden and Rasmussen 1999; Post 2002), but the sources and extent of this variation have not been previously characterized for polar desert sites. We found significantly higher d15N values in organic matter of offshore sediment than in nearshore biofilms, which likely results from different biogeochemical cycling of nitrogen between zones. Offshore chironomid larvae had higher d15N values by 1.9 %, on average, compared to nearshore. Similarly, higher d15N values by 2.3 and 3.6 % were observed in primary consumers between littoral and profundal zones of lakes by Syva¨ranta et al. (2006) and Vander Zanden and Rasmussen (1999), respectively. In addition, our field estimate for d15N trophic fractionation of 1.4 % between putative organic matter sources and chironomids is considerably lower than a commonly assumed factor of 3.4 % between trophic levels. This observation is consistent with other studies that indicate lower trophic fractionation of nitrogen stable isotopes between primary consumer invertebrates and their diet (Bunn et al. 2013), including a similar fractionation factor of 1.5 % obtained in a laboratory feeding experiment with chironomids (Goedkoop et al. 2006). These two sources of d15N variation within polar desert lakes are relevant for calculations of trophic position of Arctic char.
Biomagnification of MMHg at the base of the benthic food web Our estimate that MMHg biomagnifies 11 times between benthic algae and chironomid larvae is comparable to an average trophic magnification factor (TMF) of 12 measured in lakes on Cornwallis Island by Gantner et al. (2010b). In that study, food web TMFs were determined using mercury concentrations and d15N values for three trophic levels (benthic algae, invertebrates and Arctic char), with most data for fish. In a global meta-analysis of mercury biomagnification rates in aquatic food webs, Lavoie et al. (2013) also found an average TMF of 12 for MMHg in polar fresh waters. This level of biomagnification was higher than TMFs for temperate latitude (mean TMF = 8) and tropical fresh waters (mean TMF = 4) (Lavoie et al. 2013). The processes leading to greater biomagnification at high latitudes are unclear but may be
123
Polar Biol (2014) 37:1785–1796
related to slower growth rates and lower food quality or quantity (Karimi et al. 2007; Lavoie et al. 2013). Our study suggests that processes at the base of the food web contribute to the sensitivity of polar fresh waters to MMHg, in addition to high biomagnification between slow-growing fish and their prey (Gantner et al. 2010b). We estimated the biomagnification of MMHg to chironomids using macroscopic forms of benthic algae (filaments and Nostoc spheres). They were used as a proxy for algal MMHg concentrations even though those forms are not readily consumed by chironomids. Gut contents of chironomids from polar desert lakes contain microscopic items, mainly diatoms and sediment detritus (the latter may originate from terrestrial or autochthonous sources) (Che´telat et al. 2010). It remains a challenge to isolate microscopic diet items of invertebrates and measure the MMHg concentrations. A large body of evidence from stable isotopes shows that chironomids and other benthic invertebrates can be highly selective feeders and have specialized diets of different microbes and organic matter sources (Grey et al. 2004; Hershey et al. 2006; Reuss et al. 2013). This diet selectivity may explain some of the taxonomic variation in MMHg bioaccumulation, particularly between the Trichoptera and Chironominae chironomids. Mercury bioaccumulation in a warming Arctic The Arctic is undergoing major environmental change (ACIA 2005; Furgal and Prowse 2009) that will likely impact the cycling and fate of mercury (Stern et al. 2012). Climate change may potentially affect processes of mercury transport to Arctic ecosystems, its biogeochemical transformations, and food web bioaccumulation (Stern et al. 2012). Within lakes, anticipated environmental changes include warmer water temperatures, a longer icefree period, increased watershed inputs of nutrients and organic matter, and the onset of thermal stratification, which may have profound influences on lake ecology, productivity and species composition (Prowse et al. 2006; Wrona et al. 2006). The net effect of these environmental changes on MMHg bioaccumulation at the base of food webs in polar desert lakes remains unclear. However, given the rapid rate at which environmental changes are occurring in our study lakes (Michelutti et al. 2003), the findings described herein should be considered within that broader context. Implications for understanding MMHg bioaccumulation in Arctic char Five of the six study lakes had similar MMHg concentrations in chironomids. Interestingly, other research indicates that mercury concentrations in Arctic char from those lakes
Polar Biol (2014) 37:1785–1796
vary several-fold (Muir et al. 2005; Gantner et al. 2010b). Gantner et al. (2010a) found that length-adjusted THg concentrations in Arctic char (measured from 2005 to 2007) were significantly different among lakes (Amituk [ Char [ Plateau, Resolute, Meretta [ Small). Therefore, much of the among-lake variation in Arctic char mercury concentrations may be due to differences in food web structure or fish bioenergetics, rather than the supply of MMHg. We found that Amituk Lake had the highest chironomid MMHg concentrations, which is consistent with published observations of elevated mercury in char from that lake (up to 3.9 lg g-1 wet wt) (Muir et al. 2005). While further research is needed to explain among-lake differences in char mercury concentrations, this study highlights the importance of characterizing bioaccumulation at the base of the food web for determining the dominant processes controlling MMHg levels in higher level consumers. Bottom trophic levels provide information on MMHg exposure that is useful to evaluate and track impacts of atmospheric mercury deposition and environmental change on polar desert lakes. Acknowledgments This research was funded by the Northern Contaminants Program (Aboriginal Affairs and Northern Development Canada). We thank the Polar Continental Shelf Project for logistical and helicopter support to conduct the field program at Resolute Bay. The Resolute Bay Hunters and Trappers Association kindly provided permission to sample local lakes. Assistance in the field from Catherine Girard, Brian Dimock and Pilipoosie Iqaluk was greatly appreciated. We thank three anonymous reviewers for helpful comments on an earlier draft of the manuscript.
References ACIA (2005) Arctic climate impact assessment. Cambridge University Press, New York. ISBN-13 978-0-521- 86509 AMAP (2011) AMAP assessment 2011: Mercury in the Arctic. Arctic Monitoring and Assessment Programme (AMAP), Oslo, Norway, pp xiv ? 193 Amyot M, Lean D, Mierle G (1997) Photochemical formation of volatile mercury in high Arctic lakes. Environ Toxicol Chem 16(10):2054–2063 Antoniades D, Michelutti N, Quinlan R, Blais JM, Bonilla S, Douglas MSV, Pienitz R, Smol JP, Vincenta WF (2011) Cultural eutrophication, anoxia, and ecosystem recovery in Meretta Lake, High Arctic Canada. Limnol Oceanogr 56(2):639–650 Bunn SE, Leigh C, Jardine TD (2013) Diet-tissue fractionation of d15N by consumers from streams and rivers. Limnol Oceanogr 58(3):765–773 Cai Y, Tang G, Jaffe´ R, Jones R (1997) Evaluation of some isolation methods for organomercury determination in soil and fish samples by capillary gas chromatography—atomic fluorescence spectrometry. Int J Environ Anal Chem 68(3):331–345 Callaghan TV, Bjo¨rn LO, Chapin FS, Chernov Y, Christensen TR, Huntley B, Ims R, Johansson M, Riedlinger DJ, Jonasson S, Matveyeva N, Oechel W, Panikov N, Shaver G (2005) Arctic tundra and polar desert ecosystems. ACIA. Arctic climate impact assessment. Cambridge University Press, New York, pp 243–352
1795 Che´telat J, Amyot M, Cloutier L, Poulain A (2008) Metamorphosis in chironomids, more than mercury supply, controls methylmercury transfer to fish in High Arctic lakes. Environ Sci Technol 42(24):9110–9115. doi:10.1021/es801619h Che´telat J, Cloutier L, Amyot M (2010) Carbon sources for lake food webs in the Canadian High Arctic and other regions of Arctic North America. Polar Biol 33(8):1111–1123 Che´telat J, Amyot M, Cloutier L (2012) Shifts in elemental composition, methylmercury content and d15N ratio during growth of a High Arctic copepod. Freshw Biol 57(6):1228–1240 Dietz R, Sonne C, Basu N, Braune B, O’Hara T, Letcher RJ, Scheuhammer T, Andersen M, Andreasen C, Andriashek D, Asmund G, Aubail A, Baagøe H, Born EW, Chan HM, Derocher AE, Grandjean P, Knott K, Kirkegaard M, Krey A, Lunn N, Messier F, Obbard M, Olsen MT, Ostertag S, Peacock E, Renzoni A, Rige´t FF, Skaare JU, Stern G, Stirling I, Taylor M, Wiig T, Wilson S, Aars J (2013) What are the toxicological effects of mercury in Arctic biota? Sci Total Environ 443:775–790 Doi H, Kikuchi E, Takagi S, Shikano S (2006) Selective assimilation by deposit feeders: experimental evidence using stable isotope ratios. Basic Appl Ecol 7(2):159–166 Donaldson SG, Van Oostdam J, Tikhonov C, Feeley M, Armstrong B, Ayotte P, Boucher O, Bowers W, Chan L, Dallaire F, Dallaire R, Dewailly E, Edwards J, Egeland GM, Fontaine J, Furgal C, Leech T, Loring E, Muckle G, Nancarrow T, Pereg D, Plusquellec P, Potyrala M, Receveur O, Shearer RG (2010) Environmental contaminants and human health in the Canadian Arctic. Sci Total Environ 408(22):5165–5234 Fry B (2006) Stable Isotope Ecology. Springer, New York Furgal C, Prowse T (2009) Climate impacts on Northern Canada: introduction. Ambio 38(5):246–247 Gallagher CP, Dick TA (2010) Trophic structure of a landlocked Arctic char Salvelinus alpinus population from southern Baffin Island, Canada. Ecol Freshw Fish 19(1):39–50 Gantner N, Muir DC, Power M, Iqaluk D, Reist JD, Babaluk JA, Meili M, Borg H, Hammar J, Michaud W, Dempson B, Solomon KR (2010a) Mercury concentrations in landlocked Arctic char (Salvelinus alpinus) from the Canadian Arctic. Part II: influence of lake biotic and abiotic characteristics on geographic trends in 27 populations. Environ Toxicol Chem 29(3):633–643. doi:10. 1002/etc.96 Gantner N, Power M, Iqaluk D, Meili M, Borg H, Sundbom M, Solomon KR, Lawson G, Muir DC (2010b) Mercury concentrations in landlocked Arctic char (Salvelinus alpinus) from the Canadian Arctic. Part I: insights from trophic relationships in 18 lakes. Environ Toxicol Chem 29(3):621–632. doi:10.1002/etc.95 ˚ kerblom N, Demandt MH (2006) Trophic fractionGoedkoop W, A ation of carbon and nitrogen stable isotopes in Chironomus riparius reared on food of aquatic and terrestrial origin. Freshw Biol 51(5):878–886 Grey J, Kelly A, Jones RI (2004) High intraspecific variability in carbon and nitrogen stable isotope ratios of lake chironomid larvae. Limnol Oceanogr 49(1):239–244 Hammerschmidt CR, Fitzgerald WF, Lamborg CH, Balcom PH, Tseng CM (2006) Biogeochemical cycling of methylmercury in lakes and tundra watersheds of Arctic Alaska. Environ Sci Technol 40(4):1204–1211 Hershey AE, Beaty S, Fortino K, Kelly S, Keyse M, Luecke C, O’Brien WJ, Whalen SC (2006) Stable isotope signatures of benthic invertebrates in arctic lakes indicate limited coupling to pelagic production. Limnol Oceanogr 51(1):177–188 Hintelmann H, Keppel-Jones K, Evans RD (2000) Constants of mercury methylation and demethylation rates in sediments and comparison of tracer and ambient mercury availability. Environ Toxicol Chem 19(9):2204–2211
123
1796 Hobson KA, Welch HE (1995) Cannibalism and trophic structure in a high Arctic lake: insights from stable-isotope analysis. Can J Fish Aquat Sci 52(6):1195–1201 Ings NL, Hildrew AG, Grey J (2010) Gardening by the psychomyiid caddisfly Tinodes waeneri: evidence from stable isotopes. Oecologia 163(1):127–139 Jones RI, Carter CE, Kelly A, Ward S, Kelly DJ, Grey J (2008) Widespread contribution of methane-cycle bacteria to the diets of lake profundal chironomid larvae. Ecology 89(3):857–864 Jorgenson JK, Welch HE, Curtis MF (1992) Response of Amphipoda and Trichoptera to lake fertilization in the Canadian Arctic. Can J Fish Aquat Sci 49(11):2354–2362 Karimi R, Chen CY, Pickhardt PC, Fisher NS, Folt CL (2007) Stoichiometric controls of mercury dilution by growth. Proc Natl Acad Sci USA 104(18):7477–7482. doi:10.1073/pnas.0611261104 Lavoie RA, Jardine TD, Chumchal MM, Kidd KA, Campbell LM (2013) Biomagnification of mercury in aquatic food webs: a worldwide meta-analysis. Environ Sci Technol 47(23):13385–13394. doi:10.1021/es403103t Lehnherr I, St. Louis VL, Kirk JL (2012) Methylmercury cycling in high arctic wetland ponds: controls on sedimentary production. Environ Sci Technol 46(19):10523–10531 Loseto LL, Lean DRS, Siciliano SD (2004) Snowmelt sources of methylmercury to high arctic ecosystems. Environ Sci Technol 38(11):3004–3010. doi:10.1021/es035146n Markager S, Vincent WF, Tang EPY (1999) Carbon fixation by phytoplankton in high Arctic lakes: implications of low temperature for photosynthesis. Limnol Oceanogr 44(3):597–607 Michelutti N, Douglas MSV, Smol JP (2003) Diatom response to recent climatic change in a high arctic lake (Char Lake, Cornwallis Island, Nunavut). Glob Planet Change 38:257–271 Muir D, Wang X, Bright D, Lockhart L, Ko¨ck G (2005) Spatial and temporal trends of mercury and other metals in landlocked char from lakes in the Canadian Arctic archipelago. Sci Total Environ 351–352:464–478 NCP (2012) Canadian Arctic contaminants assessment report III: Mercury in Canada’s North. Northern Contaminants Program (NCP), Aboriginal Affairs and Northern Development Canada, Ottawa, pp xxiii ? 276 Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83(3):703–718 Premke K, Karlsson J, Steger K, Gudasz C, von Wachenfeldt E, Tranvik LJ (2010) Stable isotope analysis of benthic fauna and their food sources in boreal lakes. J N Am Benthol Soc 29(4):1339–1348
123
Polar Biol (2014) 37:1785–1796 Prowse TD, Wrona FJ, Reist JD, Gibson JJ, Hobbie JE, Le´vesque LMJ, Vincent WF (2006) Climate change effects on hydroecology of arctic freshwater ecosystems. Ambio 35(7):347–358 Reuss NS, Hamerlı´k L, Velle G, Michelsen A, Pedersen O, Brodersen KP (2013) Stable isotopes reveal that chironomids occupy several trophic levels within West Greenland lakes: implications for food web studies. Limnol Oceanogr 58(3):1023–1034 Schindler DW, Welch HE, Kalff J, Brunskill GJ, Kritsch N (1974) Physical and chemical limnology of Char Lake, Cornwallis Island (75 N Lat.). J Fish Res Board Can 31:585–607 Stern GA, Macdonald RW, Outridge PM, Wilson S, Che´telat J, Cole A, Hintelmann H, Loseto LL, Steffen A, Wang F, Zdanowicz C (2012) How does climate change influence arctic mercury? Sci Total Environ 414:22–42 Stoeva MK, Aris-Brosou S, Pelletier P, Amyot M, Hintelmann H, Che´telat J, Poulain A (2013) Microbial community structure in lake and wetland sediments from a high Arctic polar desert revealed by targeted transcriptomics. PLoS One 9(3):e89531. doi:10.1371/journal.pone.0089531 Syva¨ranta J, Ha¨ma¨la¨inen H, Jones RI (2006) Within-lake variability in carbon and nitrogen stable isotope signatures. Freshw Biol 51(6):1090–1102 Tian W, Egeland GM, Sobol I, Chan HM (2011) Mercury hair concentrations and dietary exposure among Inuit preschool children in Nunavut, Canada. Environ Int 37(1):42–48 Tsui MTK, Wang WX (2004) Uptake and elimination routes of inorganic mercury and methylmercury in Daphnia magna. Environ Sci Technol 38(3):808–816 Vander Zanden MJ, Rasmussen JB (1999) Primary consumer d13C and d15N and the trophic position of aquatic consumers. Ecology 80(4):1395–1404 Vincent WF, MacIntyre S, Spigel RH, Laurion I (2008) The physical limnology of high latitude lakes. In: Vincent WF, LaybournParry J (eds) Polar Lakes and Rivers—limnology of Arctic and Antarctic aquatic ecosystems. Oxford University Press, UK, pp 65–81 Welch HE (1976) Ecology of Chironomidae (Diptera) in a polar lake. J Fish Res Board Can 33:227–247 Welch HE, Kalff J (1974) Benthic photosynthesis and respiration in Char Lake. J Fish Res Board Can 31:609–620 Wrona FJ, Prowse TD, Reist JD, Hobbie JE, Le´vesque LMJ, Vincent WF (2006) Climate change effects on aquatic biota, ecosystem structure and function. Ambio 35(7):359–369
