ORIGINAL PAPER

Ecological determinants of methylmercury bioaccumulationin benthic invertebrates of polar desert lakes

John Chetelat • 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

� @Her Majesty the Queen in right of Canada 2014

Abstract We investigated concentrations of monometh-

ylmercury (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 infor-

mation 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 (Chiro-

nomidae and Trichoptera). We also estimated MMHg bio-

magnification between benthic algae and invertebrates.

Similar MMHg concentrations of chironomid larvae in

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 (Diamesi-

nae, Chironominae) and Trichoptera. Higher MMHg con-

centrations 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 environ-

ment is in an inorganic form, whereas organic monom-

ethylmercury (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

J. Chetelat (&)

National Wildlife Research Centre, Environment Canada,

Ottawa, ON K1A 0H3, Canada

e-mail: john.chetelat@ec.gc.ca

A. J. Poulain

Department of Biology, University of Ottawa, Ottawa, ON,

Canada

M. Amyot

Groupe de recherche interuniversitaire en limnologie, and Centre

d’etudes nordiques, Departement de sciences biologiques,

Universite de Montreal, Montreal, QC, Canada

L. Cloutier

Collection entomologique Ouellet-Robert, Departement de

sciences biologiques, Universite de Montreal, Montreal,

QC H3C 3J7, Canada

H. Hintelmann

Environmental Resource Studies Program, Department of

Chemistry, Trent University, Peterborough, ON, Canada

123

Polar Biol (2014) 37:1785–1796

DOI 10.1007/s00300-014-1561-3

environmental monitoring in the Canadian Arctic indicates

that mercury concentrations have been increasing in some

animal populations in recent decades (NCP 2012). Infor-

mation 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 spe-

cies 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 (Chetelat 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. Fer-

tilized 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 bio-

logical process that concentrated MMHg in adults by up to

three times relative to immature stages (Chetelat et al. 2008).

Environmental characteristics (specifically drainage basin

size, mercury levels in water and sediment, water tempera-

ture, and dissolved organic carbon) also explained a small

portion of differences in chironomid MMHg concentrations

among High Arctic lakes and ponds (Chetelat et al. 2008).

The influence of ecological factors such as habitat pref-

erence, 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

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; Syvaranta 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 concentra-

tions 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 con-

ducive 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 preda-

tor) 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 lati-

tude, in Nunavut, Canada) have been the focus of consid-

erable research on mercury cycling over the last two

decades (Amyot et al. 1997; Loseto et al. 2004; Muir et al.

2005; Chetelat et al. 2008; Gantner et al. 2010b), and

several lakes are monitored for temporal mercury trends

under the Northern Contaminants Program of the Gov-

ernment of Canada (NCP 2012). The overall objective of

this study was to examine the influence of ecological fac-

tors 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 chirono-

mids 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

1786 Polar Biol (2014) 37:1785–1796

123

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) Maximum depth (m)

Amituk 75�02044 93�47015 0.38 26.50 43

Char 74�42016 94�52056 0.53 3.47 27.5

Meretta 74�41036 94�59038 0.26 8.71 12

Plateau 74�48036 95�12000 0.70 6.33 14

Resolute 74�41031 94�56044 1.18 17.03 22

Small 74�45037 95�03035 0.14 1.50 11

West Longitude

Nor

th L

atitu

de

Ellesmere Island

Baffin

Island

Victoria

Island

Cornwallis Island

Resolute Bay

Amituk

Plateau Small

Char

Resolute

Meretta

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

Polar Biol (2014) 37:1785–1796 1787

123

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 aver-

age = -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 tempera-

tures 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) (Chetelat 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 near-

shore 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 snow-

melt water for much of the summer (identified as inflow #3

in Schindler et al. (1974)), was also sampled for chirono-

mid 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 con-

tained 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 dif-

ferent stations within a lake were treated as separate

replicates. For most samples, no separation of chironomid

taxa was conducted. However, when sufficient amounts of

larvae were available, individuals were separated by sub-

family (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 Montreal). 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 compar-

ison 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 near-

shore 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 inver-

tebrates (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

1788 Polar Biol (2014) 37:1785–1796

123

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 con-

centrations below detection. The relative standard devia-

tion 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 off-

shore 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 sul-

fate ? 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 concen-

trations 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.

Results

Among- and within-lake differences in chironomid

MMHg concentrations

The study lakes had similar average log MMHg concen-

trations 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 Am-

ituk 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 off-

shore 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

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

Polar Biol (2014) 37:1785–1796 1789

123

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

results suggest that water depth did not influence the

diet of chironomids, which could explain their compa-

rable 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

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

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 Zone N MMHg (ng g-1) N d13C (%) d15N (%)

Amituk Nearshore 1 44 – –

Offshore 7 184 ± 77 7 -22.2 ± 0.9 5.6 ± 0.3

Char Nearshore 4 37 ± 8 3 -27.1 ± 1.7 3.4 ± 0.5

Offshore 3 36 ± 18 1 -25.7 5.4

Inflow 2 37 ± 2 – –

Meretta 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

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)

1790 Polar Biol (2014) 37:1785–1796

123

r = 0.72, P = 0.013, N = 11; Fig. 5b). Trophic fraction-

ation of d15N was estimated between putative organic

matter sources and chironomid larvae (excluding samples

of a potentially predatory taxon), giving a mean fraction-

ation 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 chi-

ronomid 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 chir-

onomids) 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 com-

parison. 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 concen-

trations 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 chi-

ronomid larvae was calculated using the MMHg concen-

trations 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

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

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

Polar Biol (2014) 37:1785–1796 1791

123

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

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 ben-

thic invertebrate MMHg concentrations. Further, the bio-

magnification 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 chi-

ronomid d13C values were less negative than those for

planktonic invertebrates (zooplankton d13C = -33 to

-28 %) measured in Chetelat et al. (2012). Highly nega-

tive 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,

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 Zone N MMHg (ng g-1) N d13C (%) d15N (%)

Amituk Trichoptera Nearshore 1 21 – – –

Diamesinae Offshore 1 217 – – –

Char 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

Meretta Chironominae Nearshore 1 37 1 -20.4 5.1

Diamesinae 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

Small 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

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

Lake N MMHg (ng g-1) 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

1792 Polar Biol (2014) 37:1785–1796

123

profundal chironomids did not likely consume significant

amounts of methanogenic bacteria or settled phytoplank-

ton, 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 chir-

onomids consume primarily benthic algae, which is enri-

ched in 13C (Chetelat 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 trans-

parent waters which allow for benthic algal primary pro-

duction 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 sedi-

mentation rates of planktonic organic matter are likely very

low. In addition, a molecular characterization of the sedi-

ment 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 homoge-

neous 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 (Chetelat

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 (Le-

hnherr 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

surface sediment of seven cores (collected at water depths

of 6–40 m) as compared to the other lakes. Thus, the ele-

vated 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 envi-

ronmental 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 chiron-

omid 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 con-

sume other chironomids as prey (Chetelat et al. 2010) and

that higher chironomid MMHg concentrations are corre-

lated with the presence of Diamesinae in taxon-pooled

samples (Chetelat 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 inclu-

sion of the subfamily Diamesinae. We examined among-

lake and within-lake differences in chironomid MMHg

concentrations using taxon-pooled samples, and taxonomic

composition may have contributed to minor sample varia-

tion. Nevertheless, the pooling of taxa did not likely affect

our overall conclusions because large Diamesinae larvae

were not abundant. Between lake-comparisons of caddis-

flies and Chironominae, and offshore-nearshore compari-

sons 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 bio-

diversity and logistical challenges) although significant

Polar Biol (2014) 37:1785–1796 1793

123

differences were evident when data were pooled across

lakes. Further research is warranted to investigate in more

detail taxonomic variation in invertebrate MMHg bioac-

cumulation 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 dif-

ferent 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 Syvaranta 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 con-

siderably 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 inver-

tebrates and their diet (Bunn et al. 2013), including a

similar fractionation factor of 1.5 % obtained in a labo-

ratory 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 mea-

sured 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, La-

voie et al. (2013) also found an average TMF of 12 for

MMHg in polar fresh waters. This level of biomagnifica-

tion 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

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 con-

tribute 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 chir-

onomids using macroscopic forms of benthic algae (fila-

ments 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)

(Chetelat 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 tax-

onomic 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 mer-

cury 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 ice-

free 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 occur-

ring 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 concentra-

tions in chironomids. Interestingly, other research indicates

that mercury concentrations in Arctic char from those lakes

1794 Polar Biol (2014) 37:1785–1796

123

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 bioaccumula-

tion at the base of the food web for determining the

dominant processes controlling MMHg levels in higher

level consumers. Bottom trophic levels provide informa-

tion on MMHg exposure that is useful to evaluate and track

impacts of atmospheric mercury deposition and environ-

mental change on polar desert lakes.

Acknowledgments This research was funded by the Northern

Contaminants Program (Aboriginal Affairs and Northern Develop-

ment 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.

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