Manual 18104346

Manual 18104346
Environmental Toxicology and Chemistry, Vol. 28, No. 7, pp. 1480–1492, 2009
䉷 2009 SETAC
Printed in the USA
0730-7268/09 $12.00 ⫹ .00
†Canadian Rivers Institute and Department of Biology, University of New Brunswick, Saint John, New Brunswick E2L 4L5, Canada
‡Canadian Rivers Institute and Department of Biology, §Faculty of Forestry and Environmental Management, University of New Brunswick,
Fredericton, New Brunswick E3B 5A3, Canada
( Received 24 September 2008; Accepted 12 January 2009)
Abstract—Water striders (Hemiptera: Gerridae) have been considered as a potential sentinel for mercury (Hg) contamination of
freshwater ecosystems, yet little is known about factors that control Hg concentrations in this invertebrate. Striders were collected
from 80 streams and rivers in New Brunswick, Canada, in August and September of 2004 through 2007 to assess the influence of
factors such as diet, water chemistry, and proximity to point sources on Hg concentrations in this organism. Higher than average
Hg concentrations were observed in the southwest and Grand Lake regions of the province, the latter being the location of a coalfired power plant that is a source of Hg (⬃100 kg annually), with elevated Hg concentrations in the lichen Old Man’s Beard (Usnea
spp.) in its immediate vicinity. Across all streams, pH and total organic carbon of water were relatively weak predictors of strider
Hg concentrations. Female striders that were larger in body size than males had significantly lower Hg concentrations within sites,
suggestive of growth dilution. There was no relationship between percent aquatic carbon in the diet and Hg concentrations in
striders. For those striders feeding solely on terrestrial carbon, Hg concentrations were higher in animals occupying a higher trophic
level. Mercury concentrations were highly variable in striders collected monthly over two growing seasons, suggesting short-term
changes in Hg availability. These measurements highlight the importance of considering both deposition and postdepositional
processes in assessing Hg bioaccumulation in this species. They also suggest that striders may be more appropriate as a terrestrial
rather than an aquatic Hg sentinel, underscoring the importance of understanding the origin of food for organisms used in contaminant
Power plant
Growth dilution
Trophic level
the effect and extent of point source emissions on the surrounding environment and the relative importance of atmospheric deposition compared with other abiotic and biotic processes, such as water chemistry and food web characteristics.
Although mathematical models predict that reduced emissions
from point sources such as coal-fired power plants will result
in reductions in animal tissue concentrations [8] and certain
studies have shown such concentration declines after emissions
reductions [8,9], these decreases may not always be achieved
due to complexities associated with water chemistry and biology [10]. Given the logistic issues surrounding the collection
and analysis of fish samples for Hg on a broad geographic
scale, water striders are envisioned as a rapid means of assessing spatial patterns in Hg bioaccumulation in lotic food
webs [7]. Specifically, herein water striders were sampled to
identify potential Hg hotspots and areas of concern, as have
been reported previously for northeastern North America [8].
The present study examined spatial variability and potential
factors that influence Hg concentrations in water striders. First,
preliminary sampling was conducted on a broad geographic
scale in New Brunswick, Canada, to assess the variation in
strider Hg concentrations across the landscape. A study was
then designed to assess spatial patterns in Hg deposition relative to a coal-fired power plant in New Brunswick, Canada,
and determine if Hg concentrations in water striders reflect
local deposition [11]. Lichen (Usnea spp., Old Man’s Beard)
were used as a second sentinel species because they are indicators of heavy metal contamination via atmospheric deposition [12]. A variety of other factors were examined as
possible determinants of water strider Hg concentrations. For
Mercury (Hg) contamination of freshwater ecosystems remains a major problem in industrialized nations, with deposition from natural and anthropogenic sources and subsequent
methylation leading to high Hg concentrations in fishes [1].
Human and wildlife health concerns surrounding consumption
of Hg-contaminated fishes require considerable research and
monitoring efforts by government agencies [2], and losses of
Hg-contaminated products (mainly fish and marine mammals)
are estimated at billions of dollars globally [3].
Environmental sentinels hold great promise in providing
efficient and ecologically relevant information on the regional
and global distribution of contaminants [4]. Ideal characteristics of sentinel species include wide distribution, limited
home range, well-known life history, moderate to high abundance, and simple taxonomic identification [4]. The predaceous water strider (Hemiptera: Gerridae) meets many of these
criteria. One species, Aquarius remigis Say, is common and
abundant on the surface film of streams and rivers across North
America [5], has a home range that is restricted to approximately 100 m [6], and has Hg concentrations that have been
correlated with those in small brook trout Salvelinus fontinalis,
an important recreational fish species [7].
Despite an improved understanding of the Hg cycle over
the past 40 years, several fundamental questions remain about
* To whom correspondence may be addressed
( The current address of T.D. Jardine is Australian Rivers Institute, Griffith University, Nathan, Brisbane, Queensland 4111, Australia.
Published on the Web 2/12/2009.
Mercury in water striders
Environ. Toxicol. Chem. 28, 2009
Fig. 1. Location of streams sampled in 2004 (open circles) and 2005 (solid circles) (A) and in 2006 and 2007 (B) in New Brunswick, Canada.
Point sources of Hg are marked with stars in the Belledune region and the Grand Lake region, and the Grand Lake power plant sits at the center
of the bull’s-eye in the years 2006 and 2007. Panel A acronyms all refer to recreational fishing areas designated by the Department of Natural
Resources: SW ⫽ Southwest; LSJ ⫽ Lower St. John; IBF ⫽ Inner Bay of Fundy; USJ ⫽ Upper St. John; MIR ⫽ Miramichi; SE ⫽ Southeast;
REST ⫽ Restigouche; and CHA ⫽ Chaleur.
example, increased acidity [13] and dissolved organic matter
content [14] of water, changes in growth and activity rates
[15,16], and differences in feeding ecology [17] can all modulate Hg concentrations in aquatic biota. Differences in growth
patterns among water strider species and sexes within sites
were also examined to explain possible differences in Hg concentrations across sites. Mercury data from all sites were also
compared with previously reported [18] stable isotope ratios
of carbon (13C/12C or ␦13C) and nitrogen (15N/14N or ␦15N) as
indicators of food source pathway (aquatic vs terrestrial) and
trophic level, respectively, to assess the effects of feeding ecology on Hg concentrations in striders. Finally, seasonal and
interannual changes in Hg concentrations were measured at
four index sites sampled biweekly over two growing seasons.
All of these measurements were done to assess the utility of
water striders as environmental Hg sentinels and determine
the relative importance of atmospheric deposition and instream processes in affecting Hg concentrations in this organism.
Water striders were collected with hand nets from a total
of 80 streams in New Brunswick (NB) from 2004 to 2007. In
2004, water striders were collected from 42 randomly selected
streams (Fig. 1A) that represented the eight recreational fishing
areas designated by the provincial authority (NB Department
of Natural Resources) and the major drainage basins in the
province; these data were used to establish regional patterns
Environ. Toxicol. Chem. 28, 2009
of Hg concentrations. These sites were generally forested firstto sixth-order streams and rivers with cobble or gravel bottoms.
Although four species of water strider were present at some
sites (Aquarius remigis, Metrobates hesperius, Limnoporus
sp., and Gerris comatus), adult A. remigis was the most common, and collections focused primarily on this species. Metrobates hesperius was also collected at nine of the sites in
2004, but it only occurred in sympatry with A. remigis at one
In 2005, A. remigis was collected from 13 streams, with
preliminary sampling directed at locations near two coal-fired
power plants operated by NB Power in Belledune (northern
NB) and Grand Lake (south-central NB) (Fig. 1A). The Grand
Lake plant, burning local high S coal (S content ⫽ 6.6% [19])
at approximately 230,000 to 430,000 metric tons per year, is
a source of low-grade sulfur dioxide [20] and also emits approximately 100 kg of Hg per annum [21]. The Belledune
plant releases approximately 13 kg of Hg per annum (http://, [21]), but the presence of two other local
sources (a metal smelter emitting ⬃30 kg Hg per annum and
a chlor-alkali plant emitting ⬃32 kg Hg per annum [22]) add
further amounts of Hg to the local environment.
In 2006, a bull’s-eye design was used to select sampling
sites and map Hg concentrations in water striders and Usnea
spp., with the Grand Lake generating station at the center of
the bull’s-eye (Fig. 1B). Repeat sampling of the sites within
the bull’s-eye was done in 2007, due to an operational shutdown at the station in 2006 during the months of July and
August (A. Bielecki, NB Power Corporation, Fredericton, New
Brunswick, personal communication). A minimum of one site
was chosen within each section delineated by six radii (10,
20, 30, 50, 100, and ⬎100 km) and eight compass directions,
yielding a total of 60 sites per year (Fig. 1B). Water striders
were collected in August or September from these sites, with
A. remigis again being the main target species (collected at
51 sites); M. hesperius was also collected when present (9
sites). Old Man’s Beard was randomly sampled from two to
five trees per site at the same locations sampled for water
striders (Fig. 1B) and pooled into a single composite for analysis, for a total sample size of 60.
In all four years, water quality samples were collected during
baseflow conditions (August and September, n ⫽ 1/site). In
2004, water samples were analyzed for total Hg and total organic
carbon (TOC) with a Tekran Model 2600 (U.S. Environmental
Protection Agency Method 1631,
waterscience/methods/method/mercury/1631b-fs.html) and a
Technicon TrAAcs 800 auto analyzer, respectively. In 2005,
water samples were analyzed for total Hg at the Environment
Canada Laboratory in Moncton, NB, by flameless atomic absorption spectrometry after oxidation to inorganic mercury by
sulfuric acid, dichromate, and ultraviolet photo-oxidation and
reduction with stannous sulfate in hydroxylamine sulfate–sodium chloride solution. The detection limit was 0.02 ␮g/L. From
2005 through 2007, water samples were analyzed for pH and
TOC at the NB Department of Environment Analytical Laboratory (Fredericton, NB). Due to logistic constraints associated
with the collection of large volumes of water at remote sites,
in 2006 and 2007 water samples were not analyzed for Hg.
Also, because the pH, TOC, and Hg of water samples was not
being compared among years, no trials were performed to compare data generated by the different techniques.
In 2006 and 2007, water striders from four index sites (Corbett Brook, 45.92⬚N, 66.64⬚W; English Brook, 46.43⬚N,
T.D. Jardine et al.
66.60⬚W; McKenzie Brook, 46.22⬚N, 66.53⬚W; and Parks
Brook 45.46⬚N, 66.35⬚W) were sampled biweekly from May
to October to assess seasonal changes in Hg concentrations.
A. remigis adults and nymphs were collected at all four sites;
M. hesperius was only present at Parks Brook and was not
included in any temporal analyses.
For the strider samples collected in both 2004 and 2005,
two to three composite samples of two individuals (sexes and
wet weights not determined) per composite were analyzed for
total Hg from each site. In 2006 and 2007, male and female
striders were analyzed separately; males are readily discernable from females by inspection of genital morphology [23].
For each site, individuals were weighed to obtain wet weights,
and two to seven individuals were pooled for each sex. This
yielded a mean wet weight and a single composite Hg concentration for each sex at each site on a given date.
In the laboratory, water strider samples were freeze-dried
for a minimum of 48 h and homogenized with a mortar and
pestle. Lichen samples were cut with stainless steel scissors
into 1-cm sections and freeze-dried prior to analysis. All instruments were cleaned with 10% hydrochloric acid between
samples. All strider and lichen samples (2004–2007) were
weighed to approximately 10 mg and analyzed for total Hg
using a direct mercury analyzer (DMA 80, Milestone Microwave Laboratory Systems). The direct mercury analyzer was
routinely calibrated by analyzing a certified reference material
at varying weights to yield a calibration curve that covered
the range of Hg in the samples. Data are reported as micrograms per gram dry weight. Samples were run with two certified reference materials—DORM-2 (dogfish muscle, National
Research Council, Ottawa, ON, certified mean value Hg ⫽
4.64 ␮g/g, 95% confidence interval ⫽ 4.38–4.90 ␮g/g) and
IAEA 336 (lichen, International Atomic Energy Agency, Vienna, Austria, Hg ⫽ certified mean value ⫽ 0.20 ␮g/g, 95%
confidence interval ⫽ 0.16–0.24 ␮g/g)—for water striders and
Old Man’s Beard, respectively. Recoveries of DORM-2 (n ⫽
60) and IAEA 336 (n ⫽ 17) were 4.33 ⫾ 0.17 ␮g/g standard
deviation (SD) (93.3 ⫾ 3.6% SD) and 0.16 ⫾ 0.01 ␮g/g SD
(78.2 ⫾ 1.6% SD), respectively. The lower value for IAEA336 is likely due to the aliquot received, because the same
batch analyzed at a second lab (n ⫽ 33) yielded similar results
(mean ⫽ 0.15 ⫾ 0.01 ␮g/g, recovery ⫽ 76.5 ⫾ 3.7% SD).
Sample repeats yielded average standard deviations of 0.02
␮g/g both within (n ⫽ 24) and across (n ⫽ 25) analytical runs,
and blanks yielded Hg that was consistently less than 10% of
sample Hg. To determine if the power plant was causing increased deposition of sulfur [20] and whether S and Hg concentrations exhibited similar deposition patterns, Old Man’s
Beard samples from 2006 were also analyzed for percent S
using a LECO CNS 2000 elemental analyzer (LECO Instruments).
Mercury concentrations in water striders were compared to
their dietary habits using the previously reported percentage
of aquatic carbon (calculated using ␦13C) and ␦15N data [18].
For analysis of stable isotopes, approximately 0.2 mg of each
freeze-dried, ground sample was weighed into tin cups. Samples were analyzed with a NC2500 elemental analyzer connected to a Finnigan Delta XP mass spectrometer. Isotope data
are expressed using delta notation in per mil (‰) according
to (Rsample/Rstandard ⫺ 1) ⫻ 1,000, where R is the raw ratio of
heavy to light isotope (e.g., 13C/12C) and standards are Peedee
belemnite carbonate and atmospheric nitrogen for carbon and
Mercury in water striders
nitrogen, respectively. Accuracy and precision were monitored
with commercially available standards as described in [18].
A subset of water strider samples (A. remigis, n ⫽ 26; M.
hesperius, n ⫽ 6) was analyzed for methyl Hg. These samples
were selected from 14 sites sampled in 2005 and 2006 and
approximated the range of total Hg concentrations observed
(0.05–0.71 ␮g/g). Methyl Hg extractions were done using
methods outlined in [24]. Resultant solutions were analyzed
by gas chromatography–mass spectrometry on a Hewlett-Packard 6890 series with HP injector series 7683 following [25].
Recovery of a certified reference material (DORM-2) averaged
98 ⫾ 12% SD (range ⫽ 83–118%, n ⫽ 13).
Data were analyzed using NCSS and SYSTAT (version 9,
SPSS) software. All Hg data for striders and Usnea spp. were
log-transformed prior to analysis to reduce heteroscedasticity
and to normalize its distribution. On the basis of inspection
of a probability plot percent sulfur data for Usnea spp. were
judged to be normally distributed and hence were not transformed. To assess general patterns of strider Hg concentrations
from sampling done in 2004 and 2005, analysis of variance
(ANOVA) was used with site nested within recreational fishing
area (2004) and site nested within region (2005). Concentrations of methyl versus total Hg were compared first between
species of water striders and then between sexes using analysis
of covariance (ANCOVA, intercept representing percent methyl Hg) with methyl Hg as the dependent variable and total Hg
as the covariate. Equivalency of slopes was tested prior to
testing intercepts. Unless otherwise mentioned, ␣ was set at
0.05 for all statistical analyses.
For Old Man’s Beard data, we examined relationships between distance (independent variable) and Hg concentrations
(2006 and 2007) or percent sulfur (2006 only; dependent variables) using linear regressions. Because the same sites were
sampled in 2006 and 2007 (thus violating the assumption of
independence of samples for multiyear models) and samples
were pooled within sites, a paired t test was used to determine
differences in Old Man’s Beard Hg concentrations between
these two years. The effect of compass direction on Hg in Old
Man’s Beard was tested separately for 2006 and 2007 using
an ANCOVA, with direction (NW, NE, SE, or SW) as the
categorical variable and distance from the power plant as the
Linear regressions were used to separately test the effect
of distance from the power plant on water strider male and
female Hg concentrations in each of 2006 and 2007. Two sites
were excluded in 2007 as outliers in Hg versus distance plots,
identified by R[student] ⬎ 2. Because data were from pooled
samples, paired t tests were used to compare Hg concentrations
in striders between the latter two years. An ANCOVA was
used to test the effect of direction on strider Hg concentrations
separately for sexes and years. Linear regressions were used
to test the effect of different water chemistry variables on
strider Hg concentrations (focusing on females in 2006 and
2007 because female Hg concentrations were highly correlated
with those of males). For 2006 and 2007 data, a multiple
regression model was used to test for the effects of distance
from the power plant and pH (the most likely driver of changes
in Hg due to water quality). To examine the influence of body
size (as a surrogate for growth) on Hg concentrations, paired
t tests were used to compare Hg concentrations and body
weights between sexes within species and to compare Hg concentrations between A. remigis and M. hesperius at sites where
they coexisted. Sites were used to pair sexes and species in
Environ. Toxicol. Chem. 28, 2009
these two analyses. The influence of percent aquatic carbon
in the diet on strider Hg concentrations was tested using linear
regression (again focusing on females in 2006 and 2007 for
reasons noted above). For those sites with no contribution of
aquatic carbon to strider diet (% aquatic carbon ⫽ 0%), Hg
concentrations in striders were compared to their ␦15N as an
indicator of trophic level. For this analysis, it was assumed
that there was no variation in baseline ␦15N across sites because
terrestrial organic matter shows little variation (e.g., alder, ␦15N
⫽ ⫺1.0 ⫾ 0.5‰ SD, range ⫽ ⫺2.6 to 1.4‰, n ⫽ 92, T.D.
Jardine, unpublished data).
For the data collected at the four index sites over the growing season, results were grouped into two generations (as in
Jardine et al. [18])—the first group returned to stream surfaces
after overwintering (postwinter), and the second group was
the new generation that hatched in early summer (prewinter).
Adults sampled in the period after ice-out in the spring up to
and including the first day when a new generation of nymphs
was present (typically early July) were considered as the postwinter sample. Adults sampled for the remainder of the growing season (July–October) were made up of a new generation
and considered prewinter. This latter period also corresponded
roughly to the time period when the annual spatial sampling
(bull’s-eye) was conducted. The timing of the arrival of the
new generation, and hence the delineation of the two samples,
varied slightly from one stream to another. Originally, the intention was to examine whether Hg concentrations varied significantly over time and between sexes at the four streams that
were regularly sampled by comparing adult water strider Hg
concentrations across sampling periods using general linear
model analysis of variance (GLM-ANOVA). The GLM-ANOVA had three factors, site (random factor, Corbett Brook,
English Brook, McKenzie Brook, and Parks Brook), sex (fixed
factor, male and female), and generation (fixed factor, postand prewinter), separately for the two years of data (2006 and
2007) with a Bonferroni-adjusted probability of 0.025. However, because several interactions were significant ( p ⬍ 0.025)
in this model, including site–generation and sex–generation,
data were further separated into four groups—two generations
in each of 2006 and 2007. Within each of these groups, a
GLM-ANOVA was run with two factors—sex (fixed) and site
(random). Bonferroni-adjusted probabilities were used with ␦
⫽ 0.05/4 ⫽ 0.012.
To compare Hg concentrations in adults and nymphs, mean
values for males and females were compared to those of
nymphs for those times that they co-occurred (mainly summer)
with two factors (stage, fixed, and site, random) in a GLMANOVA with ␣ ⫽ 0.05.
Samples collected in 2004 and 2005 revealed regional patterns in water strider Hg concentrations in New Brunswick.
In 2004, total Hg concentrations in water striders ranged from
0.08 to 0.52 ␮g/g across the 31 sites. Concentrations were
typically more elevated at sites in the southwest portion of the
province, whereas the lowest concentrations occurred in the
northern half of the province (Fig. 1 and Table 1). There were
no significant differences among recreational fishing areas (F
⫽ 2.12, degrees of freedom (df) ⫽ 7, p ⫽ 0.064) but strong
differences among sites (F ⫽ 9.17, df ⫽ 26, p ⬍ 0.001) in
this year. In 2005, total Hg concentrations in striders were also
significantly different among sites (F ⫽ 25.72, df ⫽ 10, p ⬍
0.001) and had a similar range (0.06–0.52 ␮g/g) across sites
Environ. Toxicol. Chem. 28, 2009
T.D. Jardine et al.
Table 1. Total Hg (␮g/g dry wt) in water striders collected in eight
recreational fishing areas (as designated by the provincial authority
in New Brunswick, Canada, see Fig. 1) in 2004 and two regions with
point sources of Hg (Belledune and Grand Lake) in 2005 (n ⫽ number
of sites sampled): Different capital letters indicate significantly
different means (tested separately for the two years of study)
Total Hg
(standard error)
Recreational fishing area (2004)
Southwest (SW)
Lower St. John (LSJ)
Inner Bay of Fundy (IBF)
Upper St. John (USJ)
Miramichi (MIR)
Southeast (SE)
Restigouche (REST)
Chaleur (CHA)
Region (2005)
Grand Lake
0.35 (0.06)A
0.15 (0.02)B
as those collected in 2004. Concentrations were significantly
elevated in the Grand Lake region compared to the Belledune
region (F ⫽ 3.89, df ⫽ 1, p ⫽ 0.047), despite a site immediately
adjacent to the Grand Lake power plant having striders with
the lowest concentration recorded (0.06 ␮g/g) (Table 1).
Most of the Hg in water strider tissues was in the form of
methyl Hg (% methyl Hg ⫽ 87 ⫾ 15% SD, range ⫽ 59 to
132%, n ⫽ 32, both species combined; values ⬎100% stem
from analytical error associated with methyl and total Hg determination), and there were no differences in percent methyl
Hg between species (F ⫽ 0.79, df ⫽ 1, p ⫽ 0.382) or between
male and female A. remigis (F ⫽ 0.24, df ⫽ 1, p ⫽ 0.627).
A best fit equation for both sexes and both species relating
methyl Hg to total Hg was: Methyl Hg ⫽ 0.865(·)Total Hg ⫹
0.0025 (r2 ⫽ 0.96).
Mercury concentrations in Old Man’s Beard ranged from
0.06 to 0.52 ␮g/g and declined significantly with distance from
the power plant in both 2006 and 2007 ( p ⬍ 0.001, Fig. 2A).
Sulfur concentrations in 2006 also declined with distance from
the plant ( p ⫽ 0.007, Fig. 2B), although the effect was not as
strong as that observed for Hg (Hg versus distance r2 ⫽ 0.41
in 2006, 0.29 in 2007; %S versus distance r2 ⫽ 0.13, Fig. 2).
There were differences in Hg concentrations between years
for Old Man’s Beard, with 2007 having significantly higher
Fig. 2. Mean total mercury concentrations (␮g/g dry wt) (A) and mean percent sulfur (dry wt) (B) in Old Man’s Beard (Usnea spp.) relative to
distance from a coal-fired power plant in New Brunswick, Canada, in 2006 (open circles, solid best-fit line) and 2007 (solid diamonds, hatched
best-fit line).
Mercury in water striders
Environ. Toxicol. Chem. 28, 2009
Fig. 3. Mercury concentrations in female (solid diamonds, solid best-fit line) and male (open circles, hatched best-fit line) water striders (Aquarius
remigis) in New Brunswick, Canada, in 2006 (A) and 2007 (B) relative to distance from a coal-fired power plant (Fig. 1).
concentrations (t ⫽ 3.25, n ⫽ 51, p ⫽ 0.002). In 2006, there
were significant differences among directions in Hg concentrations (F ⫽ 3.38, df ⫽ 3, p ⫽ 0.024), with sites to the
northeast of the power plant having higher concentrations than
sites to the southwest. In 2007, there were no significant differences among directions (F ⫽ 2.43, df ⫽ 3, p ⫽ 0.076).
In 2006, while the power plant was not operational, Hg
concentrations in water striders showed no linear relationship
with distance from the generating station for either females (r2
⬍ 0.01, n ⫽ 52, p ⫽ 0.902) or males (r2 ⬍ 0.01, n ⫽ 51, p
⫽ 0.592) (Fig. 3A). In addition, there was no correlation between Hg concentrations in Old Man’s Beard and concentrations in male (r ⬍ 0.01, p ⬎ 0.05) or female (r ⫽ ⫺0.16, p
⬎ 0.05) water striders across sites for this year. In contrast to
2006, Hg concentrations in striders collected in 2007 significantly declined with distance from the plant in both females
(r2 ⫽ 0.12, p ⫽ 0.025, n ⫽ 49) and males (r2 ⫽ 0.21, n ⫽ 46,
p ⫽ 0.002) (Fig. 3B). Mercury concentrations significantly
increased in males (t ⫽ 1.79, n ⫽ 40, p ⫽ 0.040) but not
females (t ⫽ 0.97, n ⫽ 41, p ⫽ 0.169) in 2007 compared with
2006. Direction had no effect on Hg concentrations in males
or females in either 2006 or 2007 ( p ⬎ 0.05).
Water quality variables were inconsistent predictors of Hg
concentrations in water striders over the four years of study,
accounting for a maximum of 64% of the variation when an-
alyzed independently (Table 2). In 2004, significant relationships were observed between Hg in A. remigis and pH (r2 ⫽
0.38, p ⬍ 0.001), TOC (r2 ⫽ 0.14, p ⫽ 0.030), and conductivity
(r2 ⫽ 0.22, p ⫽ 0.003). There was no relationship between
Hg in striders and total Hg in water in 2004 for either strider
species, but in 2005 a significant positive relationship between
these two variables was observed for A. remigis (r2 ⫽ 0.64,
p ⫽ 0.008). Conductivity (r2 ⫽ 0.51, p ⫽ 0.003) and TOC (r2
⫽ 0.41, p ⫽ 0.008) were also significant predictors of Hg in
A. remigis in 2005 (Table 2). In 2006 and 2007, none of the
water quality variables was a significant predictor of Hg concentrations in A. remigis or M. hesperius (Table 2). When
analyzed in a multiple regression with pH and distance as
variables, trends were generally similar to those observed with
distance or water quality variables alone. Stream-water pH had
a weak but significant effect on female strider Hg concentrations in 2006 (r2 ⫽ 0.10, p ⫽ 0.026), whereas distance had
no effect (r2 ⫽ 0.02, p ⫽ 0.310) and males showed no effect
of pH (r2 ⫽ 0.06, p ⫽ 0.097) or distance (r2 ⫽ 0.003, p ⫽
0.682). In 2007, female Hg concentrations were not affected
by pH (r2 ⫽ 0.05, p ⫽ 0.122) or distance (r2 ⫽ 0.04, p ⫽
0.137), but males showed a significant effect of distance (r2
⫽ 0.10, p ⫽ 0.025) and not pH (r2 ⫽ 0.04, p ⫽ 0.138). When
two outliers were included in the analysis, relationships between Hg concentrations and distance or pH were nonsignif-
Environ. Toxicol. Chem. 28, 2009
T.D. Jardine et al.
Table 2. Best-fit equations relating log-transformed water strider mercury concentrations and log-transformed water quality characteristics in New
Brunswick, Canada, streams: All equations are in the form y ⫽ mx ⫹ b, n is the number of streams sampled, and TOC is total organic carbon.
The p values in italics are significant at ␣ ⫽ 0.05
Aquarius remigis
Metrobates hesperius
A. remigis
A. remigis
M. hesperius
A. remigis
Water Hg
Water Hg
Water Hg
icant ( p ⬎ 0.05) in the multiple regressions for males and
females in both 2006 and 2007.
In both 2006 and 2007, there were between-sex differences
in body size and Hg concentrations for both species of water
striders. Female water striders were consistently larger than
males (Fig. 4A). The difference in body weights between sexes
was less pronounced in A. remigis (2006, mean % difference
⫽ 23.0 ⫾ 10.8% SD, t ⫽ 15.02, n ⫽ 54, p ⬍ 0.001; 2007,
mean % difference ⫽ 21.2 ⫾ 14.8% SD, t ⫽ 10.49, n ⫽ 47,
p ⬍ 0.001; Fig. 4A) than M. hesperius (2006, mean % difference ⫽ 61.9 ⫾ 10.3% SD, t ⫽ 15.79, n ⫽ 9, p ⬍ 0.001;
2007, mean % difference ⫽ 65.4 ⫾ 6.7% SD, t ⫽ 19.33, n ⫽
7, p ⬍ 0.001; Fig. 4A). Male striders had higher Hg concentrations than females for both A. remigis (2006, mean % difference ⫽ 13.4 ⫾ 31.9% SD, t ⫽ 3.33, n ⫽ 50, p ⫽ 0.001;
2007, mean % difference ⫽ 3.8 ⫾ 7.6%, t ⫽ 5.20, n ⫽ 47, p
⬍ 0.001; Fig. 4B) and M. hesperius (2006, mean % difference
⫽ 53.7 ⫾ 36.3% SD, t ⫽ 5.65, n ⫽ 9, p ⬍ 0.001; 2007, mean
% difference ⫽ 58.1 ⫾ 8.6% SD, t ⫽ 18.41, n ⫽ 7, p ⬍ 0.001;
Fig. 4B). M. hesperius had significantly higher Hg concentrations than A. remigis (t ⫽ 2.98, n ⫽ 6 sites, p ⫽ 0.003,
data not shown) where the two species coexisted.
There was no relationship between percent aquatic carbon
in the diet and Hg concentrations in A. remigis water striders
( p ⬎ 0.05, Fig. 5A); however, these analyses were limited
given the large number of sites (n ⫽ 22 of 41 [18]) with striders
having 0% aquatic carbon in their diet. For those striders that
had aquatic carbon in their diets (2–100%), their Hg concentrations fell within the range of those animals that relied solely
on terrestrial carbon with one exception. Striders from a single
site (Clark Brook, 46.06⬚N, 65.54⬚W) had atypically high Hg
(average Hg ⫽ 2.0 ␮g/g) and were feeding mainly on aquatic
food sources (average % aquatic carbon ⫽ 79%). For those
striders with 0% aquatic carbon in their diet (i.e., entirely
terrestrial feeders), ␦15N as a measure of trophic level explained
significant variation in Hg concentrations, with high ␦15N (high
trophic level) associated with high Hg (r ⫽ 0.60, n ⫽ 25, p
⫽ 0.001, Fig. 5B). By inclusion of distance from the power
plant as a second variable in a stepwise regression, over half
of the variation was accounted for (r2 ⫽ 0.53), and both ␦15N
( p ⫽ 0.001) and distance ( p ⫽ 0.012) were significant.
Seasonal and interannual variation was high in A. remigis
Hg concentrations at the four index sites (Fig. 6), but patterns
in three of the four streams (exception Corbett Brook) were
similar, with generally lower concentrations in the late summer
or fall compared to spring. At Corbett Brook, the second generation of 2006 (adults from July to October) had Hg concentrations (0.40–0.60 ␮g/g) that remained high into the spring
of 2007 after overwintering; in contrast, the second generation
collected at this site in 2007 had lower concentrations (0.10–
0.30 ␮g/g, Fig. 6) than those from 2006. During the prewinter
period when one-time sampling at 60 sites was conducted, the
other three index sites had consistent concentrations between
years. At all index sites, concentrations of Hg in males and
females diverged in the spring, with male concentrations increasing relative to females (Fig. 6). Concentrations of Hg in
females generally remained low (0.10–0.30 ␮g/g) throughout
the growing season. Overall, there were several interactions
( p ⬍ 0.025) in the statistical analyses among sexes, generations, and sites, requiring a breakdown of the analysis. When
analyzed separately by generation and year, postwinter males
had significantly higher Hg concentrations than postwinter females in both 2006 (F ⫽ 121.59, df ⫽ 1, p ⫽ 0.002) and 2007
(F ⫽ 48.07, df ⫽ 1, p ⫽ 0.006). Hg concentrations among
sites were not significantly different during the postwinter sample in 2006 (F ⫽ 1.36, df ⫽ 3, p ⫽ 0.275), but they were
different in 2007 (F ⫽ 5.26, df ⫽ 3, p ⫽ 0.004). For prewinter
samples, Hg concentrations between sexes were not significantly different in either year (2006, F ⫽ 3.72, df ⫽ 1, p ⫽
0.149; 2007, F ⫽ 3.20, df ⫽ 1, p ⫽ 0.172) but among sites
were different during this time period in both years (2006, F
⫽ 24.76, df ⫽ 3, p ⬍ 0.001; 2007, F ⫽ 4.73, df ⫽ 3, p ⫽
0.010). In 2006, nymphs had similar concentrations to those
of adults (F ⫽ 6.40, df ⫽ 1, p ⫽ 0.086); in contrast, nymphs
collected in 2007 had significantly lower Hg concentrations
than those of adults (F ⫽ 28.51, df ⫽ 1, p ⫽ 0.013, Fig. 6).
Environ. Toxicol. Chem. 28, 2009
Mercury in water striders
Fig. 4. Correlation between male and female wet weights (A) and mercury concentrations (B) for Aquarius remigis in New Brunswick, Canada,
streams in 2006 (open diamonds, solid best-fit line) and 2007 (solid diamonds, hatched best-fit line). Inset: Correlation between male and female
wet weights (A) and mercury concentrations (B) for Metrobates hesperius in 2006 (x, solid best-fit line) and 2007 (⫹, hatched best-fit line).
The present study examined the physical, chemical, and
biological factors affecting Hg concentrations in water striders
collected across the province of New Brunswick, Canada. Variation in water strider Hg concentrations was related to distance
from the coal-fired generating station, sex, body size, and trophic level, highlighting the importance of both abiotic and
biotic factors in determining Hg concentrations in this organism. Water striders revealed regional patterns of Hg concentrations in New Brunswick that may be related to atmospheric
Hg deposition and landscape characteristics, with striders from
the northern part of the province having lowest Hg concentrations and those from the southern part having highest concentrations. These organisms feed mainly on terrestrial carbon
(⬎50% [18]); this likely explains the weaker relationship between water chemistry parameters and their Hg concentrations
and suggests that striders may be more useful as indicators of
Hg availability in the terrestrial rather than aquatic environment.
Spatial studies with sentinel species are useful for identifying areas of high and low contaminant concentrations [4].
In the present study, Hg concentrations in water striders collected in 2004 were the highest in the southwest region (Fig.
1 and Table 1) and generally decreased in a southwest to northeast direction; this pattern is consistent with studies on other
organisms in the region [8]. In the earlier study, yellow perch
(Perca flavescens) and loons (Gavia immer) from lakes in the
Lepreau region (southwest NB) showed elevated Hg concentrations. In the present study, Hg analyses of water striders
and Old Man’s Beard in 2006 and 2007 also showed elevated
concentrations (⬎0.40 ␮g/g) in the Grand Lake region in
south-central NB (Figs. 2 and 3). Areas characterized by higher
concentrations of Hg in either water striders or Usnea spp.
may potentially contain fish with high Hg concentrations and
therefore could be targeted as locations for more detailed food
web sampling.
Concentrations of Hg in both sentinel species varied considerably among sites that were at similar distances from the
coal-fired generating station, and this may be due to spatial
variability in the atmospheric deposition of this pollutant. Prior
monitoring and modeling efforts for the Grand Lake power
plant revealed that S deposition was affected by: prevailing
wind direction, which is generally directed toward the northeast; topography, with greater S deposition occurring on the
ridges than valleys located along the northeast direction; plume
height, as overall S deposition rates can be expected to decrease with increasing plume height; and variations in atmospheric stability, with highest S deposition patterns occurring
during unstable and neutral conditions [20]. Deposition of Hg
in this area could also be affected by these processes and
Environ. Toxicol. Chem. 28, 2009
T.D. Jardine et al.
Fig. 5. Mercury concentrations in Aquarius remigis in New Brunswick, Canada, streams in relation to (A) the percentage of aquatic carbon in
the diet and (B) ␦15N as an indicator of trophic level for those streams with water striders having 0% aquatic carbon in their diet.
explain some of the among-site differences for both striders
and Usnea spp. at comparable distances from the generating
station; however, examination of these processes was beyond
the limits of the present study.
We found increased concentrations of Hg in striders collected near the coal-fired power plant (⬃10–50 km away) in
2007 when compared to 2006, possibly due to the unanticipated shutdown that occurred during the first year of sampling.
Given their strong linkages to terrestrial carbon [18], the main
source of Hg for water striders would be from Hg in terrestrial
insects, which could respond relatively quickly to changes in
deposition rates via transfer from terrestrial vegetation [26].
Links have been shown to exist between Hg deposition from
precipitation and Hg concentrations in biota [27], suggesting
that on relatively large spatial and temporal scales Hg deposition may predict areas with high Hg risk [27]. Determining
the relationship between Hg deposition and Hg in water striders will require sampling across a much broader range of Hg
deposition, such as that observed across North America [27],
than that represented in this study.
In 2006 when striders and lichen were sampled during a
shutdown of the generating station, only lichen showed decreasing Hg concentrations with increasing distance from the
plant (Fig 2). In contrast, in 2007 when the plant was operational, both lichen and striders showed higher Hg concentrations at sites closer to the power plant. Differences in lifespans
of these sentinel species and responsiveness to changes in
atmospheric deposition may explain the among-year variability. Consistently high Hg concentrations in Usnea spp. nearest
the source may simply reflect a longer lifespan and Hg accumulation from previous years or decades when the power
plant was operating at a greater capacity, burning coal with a
higher concentration of Hg, or not yet using emission control
technology. Striders, meanwhile, have a one-year lifespan and
exhibit rapid turnover of their body tissues [18]; hence they
are more likely to reflect recent exposure to Hg.
Although Hg concentrations in striders and lichens were
higher closer to the coal-fired generating station at Grand Lake
(Figs. 2 and 3), maximum concentrations of Hg occurred at
different distances for these two sentinels. The major zone of
influence indicated by lichens (⬃0–10 km from the power
plant) is comparable to that found for a chlor-alkali plant in
New Brunswick [22] and for ground level measurements of
gaseous Hg around a chlor-alkali plant in Sweden [28]; in
contrast, strider Hg concentrations peaked at distances 10 to
50 km from the generating station and were poorly correlated
with Hg concentrations in Usnea spp. This suggests some
differences in Hg exposure for the two sentinels, even though
atmospheric deposition is expected to exert some control over
Hg concentrations in both Usnea spp. (via direct uptake) and
striders (indirectly via vegetation and riparian insects given
the importance of terrestrial carbon in their diets [18]). Al-
Mercury in water striders
Environ. Toxicol. Chem. 28, 2009
Fig. 6. Total mercury concentrations (␮g/g dry wt) in Aquarius remigis females (solid diamonds), males (open circles), and nymphs (open
triangles) from four New Brunswick, Canada, streams during the growing season in 2006 and 2007.
though biogeochemical cycling of Hg is not well understood
and the spatial differences between these two sentinel species
cannot be explained at present, the variability in Hg concentrations may be due to the fact that lichen take up inorganic
Hg directly through either gaseous or particulate-bound forms
whereas Hg in striders (the majority of which is methyl Hg)
would be affected by various chemical and biological processes after it is deposited onto the terrestrial or aquatic landscape and taken up into its prey. It is also possible that their
concentrations reflect the deposition of different forms of Hg;
lichen concentrations may be more reflective of particulatebound Hg deposited closer to the generating station whereas
Environ. Toxicol. Chem. 28, 2009
strider concentrations may reflect higher deposition of gaseous
forms of Hg2⫹ at distances further removed from the power
plant [11]. In the Grand Lake region, it is possible that deposition of Hg bound on particulates occurs closer to the power
plant than the deposition of gaseous Hg2⫹. Old Man’s Beard
situated to the northeast of the power plant had higher concentrations than those to the southwest in 2006, consistent with
the prevailing wind direction for the area and previously measured patterns of SO2 deposition [20]. This suggests that dry
deposition was an important source of Hg to lichens because
most precipitation (i.e., storm events) originates from the opposite direction, the northeast.
Results from this study concurred with others that have
found lower than expected Hg concentrations in aquatic consumers at sites immediately adjacent to emission sources
[29,30]. Another possible explanation for the spatial differences between strider and lichen Hg concentrations described
above may be due to decreased bioavailability of Hg to striders
living closer to the power plant. This decreased bioavailability
may be due to an inhibition of methylation of Hg or to the
concurrent deposition of selenium [30]. For example, lakes
near Sudbury, Ontario, metal smelters with high Se concentrations in water have biota with lower total and methyl Hg
concentrations than lakes far away from the smelters with low
Se concentrations [30]. Selenium can interfere with Hg binding
sites in proteins and thus limit Hg assimilation, as well as
participating in the demethylation of methyl Hg [31]. Although
previous studies have not found unusually high Se concentrations in New Brunswick wildlife (e.g., [32]), these surveys
were not conducted in the Grand Lake region. It is known,
however, that Se coaccumulates with S in sulfide-carrying coal
beds such as those of the Grand Lake area [33]. The local
burning of this coal with a high S content of 6.6% [19] would
therefore add Se as a logical associate to the local S and Hg
emission and deposition patterns, but whether this deposition
is sufficient to affect Hg uptake by striders remains to be
Water chemistry, particularly acidity and organic matter
content, is typically a determinant of Hg concentrations in
aquatic organisms [10]. Recent work on black flies, which
reside low on the food chain as primary consumers, showed
strong relationships between Hg concentrations and pH and
dissolved organic carbon [14], likely because low pH and high
dissolved organic carbon may increase the availability of Hg
to lower-trophic-level organisms [13]. In the present study,
striders had Hg concentrations that were not consistently correlated with pH and TOC of the streams across sampling years;
however, among-site variability in water chemistry is likely
inconsequential for species such as water striders that derive
the majority of their biomass from the terrestrial environment
[18] and are thus disconnected from processes occurring in
the aquatic environment.
Although relationships between Hg concentrations in water
striders and stream-water chemistry were inconsistent, there
were consistent and significant differences within sites between sexes and species. Within sites, females of both species
had larger body sizes and lower Hg concentrations than males.
Males and females hatch and grow to adulthood at the same
time, meaning that differences in size are most likely due to
differences in growth and differences in Hg between sexes
suggest growth dilution of Hg by females [16]. Furthermore,
M. hesperius attain smaller maximum body sizes than A. remigis (Figs. 4A and 5A) yet have higher Hg concentrations,
T.D. Jardine et al.
suggesting a link between growth and Hg concentrations across
species. Mercury concentrations in fishes can be affected by
differences in feeding rates, food conversion efficiency, and
growth [15]. Because A. remigis populations in NB have a
single generation each year (T.D. Jardine, unpublished data)
and A. remigis mean adult body sizes differed between sites
by 72% in males and 66% in females, among-site differences
in body size likely reflect differences in growth and food availability. These growth differences among sites could therefore
confound assessment of spatial patterns in Hg concentrations
and contribute to some of the variability observed here.
The sex difference in growth and Hg for A. remigis is not
due to source of food or trophic level, as indicated by stable
isotope studies of this species [18], but could be due to differences in feeding rate, activity level, or loss of Hg during
egg deposition. There are major differences between sexes in
the spring in activity levels, where males aggressively seek
out female partners for copulation (A. Sih, University of California, Davis, CA, USA, personal communication). Increased
activity relative to food consumption can increase Hg concentrations [15], but body size and Hg differences between
sexes are also evident during the fall. Although it is also possible that females may lose part of their Hg burden via egg
production, nymph Hg concentrations were similar to those of
breeding females at all four sites, suggesting no net loss of
Hg through this pathway. During the late summer (prewinter)
when the majority of sampling was conducted, differences
between males and females were not apparent, and Hg concentrations were generally more stable at the index sites. However, interannual variation may be high at certain sites (e.g.,
Corbett Brook where Hg concentrations in late summer 2006
were approximately 0.45 ␮g/g and in late summer 2007 were
approximately 0.15 ␮g/g). These large, unexplained changes
in Hg concentrations indicate the short-term relevance of strider contamination levels relative to longer-lived species such
as fish and possibly Usnea spp.
Stable isotope ratios suggested no link between carbon
sources and Hg concentrations in striders. The majority of
strider populations exclusively use terrestrial energy (22 of 41
sites had 0% aquatic carbon [18]), and only in rare instances
do striders derive the majority of their biomass from aquatic
prey (7 of 41 sites had ⬎50% aquatic carbon [18]). There was
no relationship between percent aquatic carbon in the strider
diet and Hg concentrations (Fig. 6A). The lack of a direct link
between carbon source and Hg concentrations in striders contrasts to previous work in lakes, where animals connected to
the pelagic zone have higher Hg concentrations than those that
use littoral energy [17]. In the present study, it was expected
that animals foraging in streams on aquatic biofilm, which is
a mixture of algae, fungi, and bacteria, may be exposed to
higher amounts of Hg due to methylation by sulfur-reducing
bacteria [34]. However, this methylation of Hg requires anoxic
conditions [34] that were rarely encountered in the well-oxygenated streams of this study (minimum dissolved oxygen
concentration for sites sampled in 2004 ⫽ 6.4 mg/L, T.D.
Jardine, unpublished data). Striders that use terrestrial carbon
can get that energy from consumption of either terrestrial insects or aquatic insects that process terrestrial particulate organic matter. These latter two sources are likely low in Hg
due to limited methylation in the terrestrial environment
[35,36]. Enhanced methylation has been shown, however, to
occur as a result of the flooding of terrestrial vegetation [37],
and the highest concentrations observed in the present study
Mercury in water striders
were at a site (Clark Brook) where strider Hg concentrations
increased from 0.4 and 0.3 ␮g/g in 2006 to 2.1 and 1.8
␮g/g in 2007 in females and males, respectively, possibly due
to flooding of the area upstream of the site by beavers in the
latter year (T.D. Jardine, personal observation). At this site,
striders were feeding on aquatic prey (aquatic C ⫽ 79%),
suggesting a link between methyl Hg release from flooded
vegetation and subsequent uptake by algae. Flooding could
therefore exert greater control over Hg concentrations in
stream biota than all other factors examined here.
For those striders that were entirely connected to the terrestrial food source pathway, trophic level explained significant variation in Hg concentrations across sites (Fig. 6B), likely reflecting biomagnification stemming from the consumption
of larger insects that are positioned higher in the food chain
[38] or cannibalism. Water striders had a high proportion of
their total Hg as methyl Hg, not surprising given their status
as obligate predators and the enhanced biomagnification of
methyl relative to inorganic mercury at higher trophic levels
[13]. Earlier studies have shown that percent methyl Hg is
related to position in the food chain for benthic invertebrates
(e.g., 35–50% methyl Hg in grazers–detritivores and 70–95%
methyl Hg in predators [39]). Because methyl Hg is the more
toxic form of Hg and subsequently of greater interest in fish,
wildlife, and human health studies [1], a high proportion of
total Hg as methyl Hg in a sentinel species is considered a
positive attribute.
The combination of environmental sentinels in this study
was useful for determining where follow-up work on Hg cycling may be warranted, because the two sentinels provided
different types of information on Hg availability to ecosystems.
Although Usnea spp. provided a clear picture of Hg deposition
near the power plant, water striders appeared more likely to
reflect the complexities associated with Hg cycling within terrestrial and aquatic food webs. Spatial assessments of Hg contamination using water striders as a sentinel will therefore
require an appreciation of their ecological characteristics (such
as potential growth rates and trophic level) as well as variation
in their Hg concentrations over the course of the growing
season. In terms of absolute abundance, sampling striders in
the fall provides the highest likelihood of capturing individuals
in sufficient numbers to analyze for total Hg and methyl Hg
and perform other analyses including stable isotopes or other
contaminants. Due to their smaller body size, rapid growth
rates, low Hg concentrations, and limited availability, nymphs
should only be sampled in studies concerned with ontogenetic
or seasonal changes in Hg concentrations. Male striders present
problems given their greater seasonal variability in Hg concentrations, particularly in the spring. This leaves females as
the best candidate for sampling given their more stable Hg
concentrations over time and their larger body size.
Overall, striders appear to have limited utility as a sentinel
for aquatic Hg contamination simply because the majority of
their biomass is derived from the terrestrial environment and
they have no secondary route of exposure to this contaminant
(i.e., waterborne Hg [40]). However, a strong connection to
the terrestrial environment may lend them to a role in linking
measured Hg concentrations with predicted atmospheric Hg
deposition, allowing a better understanding of spatial and temporal trends in Hg contamination as well as serving as indicators of Hg concentrations in other organisms that consume
terrestrial insects, such as brook trout [7]. Also, their apparent
ability to undergo rapid change in Hg concentrations (based
Environ. Toxicol. Chem. 28, 2009
on seasonal data) may make them useful as short-term indicators of Hg availability, although this would have to be tested
through controlled experimentation. Understanding the poor
correlation between Hg in striders and Hg in Usnea spp. will
also require further examination to better model the relationship among Hg emissions, deposition, and resultant concentrations in aquatic biota.
Acknowledgement—The authors thank T. Arciszewski, P. Emerson,
A. Fraser, S. Fraser, L. Giardi, K. Lippert, A. Townsend, J. Penny, T.
McMullen, C. Blanar, C. Poole, R. Keeler, P. Brett, T. Barrett, R.
Engelbertink, M. Sullivan, C. Ritchie, S. McWilliam, N. Swain, M.
Sabean, M. Nasr, D. Perkman, L. Sweeney, D. Banh, J. O’Keefe, C.
Paton, M. Savoie, A. McGeachy, O. Nwobu, E. Yumvihoze, L. Baker,
B. Wyn, E. Campbell, and E. Belyea for field and lab assistance.
Funding was provided by the O’Brien Humanitarian Trust, the NB
Wildlife Trust Fund, the NB Environmental Trust Fund, the Grand
Lake Meadows Fund, and the Natural Sciences and Engineering Research Council Discovery, Canada Graduate Scholarship, and Canada
Research Chair programs. Comments from H. Swanson, N. Burgess,
and K. Munkittrick improved the quality of this manuscript.
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