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Heavy metal, organchlorine pesticide and polychlorinated biphenyl contamination in Arctic ground squirrels (Spermophilus parrye) in northern Alaska.

(Received 5 February 1997; accepted in revised form 11 August 1997)

ABSTRACT. Heavy metal and organochlorine (OC) concentrations, including organochlorine pesticides and polychlorinated biphenyl congeners (PCBs), were determined in arctic ground squirrels (Spermophilus parryi) from three sites in the Brooks Range of northern Alaska in 1991-93. Heavy metals were present in most squirrel livers collected, with concentrations of trace elements (As, Cd, Hg, Ni, and Pb) averaging below 1 [micro]g/g wet weight. Hexachlorobenzene (HCB), p,p'-DDE, gamma hexachlorocyclohexane ([gamma]-HCH), trans-nonachlor, and PCBs 138, 153, and 170 were the most frequently detected OCs in fat and liver. Average concentrations of individual OC analytes were below 20 ng/g wet weight in liver and below 15 ng/g wet weight in fat. Rank correlations indicate that concentrations of heavy metals and of OCs accumulate in concert with one another (As, Cd, Cu, and Zn; PCBs 138, 170, and 180). Although heavy metal and OC concentrations are low relative to other areas and other arctic species, the occurrence of these compounds illustrates the global pervasiveness of persistent organic compounds and the potential for bioaccumulation in the terrestrial arctic food web.

Key words: heavy metals, organochlorine pesticides, polychlorinated biphenyls, Spermophilus parryi, northern Alaska

INTRODUCTION

Arctic terrestrial food webs are characterized by low diversity and strong interactions within communities. The low diversity reflects the fact that few species are adapted to the harsh environment; only 50 of the world's 4000 mammals are found in the Arctic, and only 8 bird species are year-round residents (Stonehouse, 1989). The faunal base of the terrestrial food web is centered on a small number of rodent species. Given the low diversity of rodent prey species, most arctic predators are opportunists, exhibiting considerable overlap in their diets (Hoffmann, 1974). Annual fluctuations in levels, longer term cycling in populations, and the coupling between prey and predator population cycles are more pronounced for arctic species than for those in temperate environments (Remmert, 1980).

The cyclic nature of arctic rodent populations potentially renders them susceptible to chronic toxicological impact. It is believed that relationships among species and external stresses (severe winters, limited food availability) are critical factors in determining the magnitude and length of population level cycles (Remmert. 1980). The influence of contaminant-induced physiological stress may exacerbate rapid population declines. Since re-establishment of the population following a population decline is dependent on the reproductive fitness of relatively few individuals and the survivorship of their offspring, the effects of agents that are genotoxic, teratogenic, or otherwise detrimental to reproduction may be amplified. Such effects on rodent populations may have repercussions for predator populations relying on small mammals as prey.

A physiological adaptation of many arctic animals to the harsh winters is the deposition and utilization of fat reserves (Batzli, 1981). Ground squirrels, in particular, rely heavily on fat deposits as an energy source during their 7 to 9 months of hibernation (Behirsch, 1984; Kenagy and Barnes, 1988). This feature renders animals susceptible both to the accumulation of persistent organic compounds and to the potential for enhanced toxicity caused by mobilization of fat reserves which may be laden with lipophilic organic compounds (Geyer et al., 1990; Shore and Douben, 1994).

Transfer of lipophilic organic compounds from prey to predator is a well-established process. Biomagnification has been documented for airborne pollutants in arctic ecosystems (Andersson et al., 1988; Norstrom et al., 1988; Larsson et al., 1990b; Kidd et al., 1995). In terrestrial systems, Larsson et al. (1990a) demonstrated that an increase in atmospheric deposition of DDT, lindane and PCBs increased uptake by plants and elevated levels in herbivores and, subsequently, in predators. Villeneuve et al. (1985) reported trophic transfer of OCs from lichen to reindeer to humans in northern Sweden.

Heavy metal contamination in arctic terrestrial food webs is also a concern. Natural geologic mineral enrichment, mining practices within the Arctic, and atmospheric transport from remote sources may all contribute to heavy metal accumulation in arctic fauna (Thomas et al., 1992; Landers et al., in press). Recent and fossil shells from the eastern Canadian Arctic show a five-fold increase in lead (Bourgoin and Risk, 1987). Cadmium, in particular, often occurs in high concentrations in arctic fauna (Shaw and Gunn, 1981 ; Snyder-Conn and Lubinski, 1993; Elkin and Bethe, 1995).

The primary goal of this research was to develop an increased understanding of contaminant loadings in select arctic fauna. Herbivorous small mammals with limited home range sizes are particularly well suited for biomonitoring of atmospherically deposited contaminants (Talmage and Walton, 1991). Among small herbivores with relatively confined home ranges, the arctic ground squirrel (Spermophilus parryi) was selected as a target species because of its ubiquitous distribution, reliance on fat reserves during hibernation, importance as a prey species (Carl, 1971: Jones and Theberge, 1983; Poole and Boag, 1988) and well-studied physiology and life history (e.g., Batzli and Sobaski, 1980; Baust and Brown, 1980: Chappell, 1981; Barnes, 1989). Arctic ground squirrels live in burrow colonies along river banks and lake basin rims, with average densities ranging from 1.5 to 8 [ha.sup.-1] in favorable habitat (Batzli and Sobaski, 1980). Animals emerge from their 8- to 9-month hibernation in April-May, breed in May, and give birth to young (5-6 per litter) in June and early July (Carl, 1971; Kiell and Millar, 1980). Ground squirrels are opportunistic herbivores, with 40 species of herbaceous dicotyledons comprising 25% to 75% of the diet. Most foraging occurs within 50 m of burrow sites (Batzli and Sobaski, 1980). Feeding during the summer is intense: by late August, percent body weight as fat can exceed 50% (Batzli and Sobaski, 1980; Kiell and Millar, 1980).

METHODS

Ground squirrels were trapped in the vicinity of Elusive, Schrader, and Feniak Lakes, located in the foothills of the Brooks Range, Alaska (Fig. 1). These sites were selected by the U.S. Environmental Protection Agency's (USEPA) Arctic Contaminants Research Program as integrated sites from which lake sediments, fish tissue, moss, and lichen samples were also analyzed for heavy metal and organochlorine contaminants (see Landers et al., 1992, 1995; Ford et al., 1995; Gubala et al., 1995; Wilson et al., 1995; Allen-Gil et al., 1997). Site selection was based on a combination of factors, including acceptable lake bathymetry for interpretation of sediment cores, occurrence of target lichen, moss, small mammal, and fish species, and geographic separation. All sites were situated in a region of high atmospheric deposition (Ford and Bedford, 1987). Although still within the foothills of the Brooks Range, Feniak Lake in northwestern Alaska is at a lower elevation than Elusive or Schrader Lakes.

[FIGURE 1 OMITTED]

Sample Collection

A combination of destructive and nondestructive sampling techniques was used. In order to provide sufficient liver mass for accurate residue analyses given the predicted low concentrations, whole livers were taken from six individuals from each site. After this quota had been achieved, nondestructive techniques were implemented as described below. All tissue samples from destructive and nondestructive procedures were treated identically following removal. Animals were trapped in Tomahawk "skunk special" live traps, located in rodent runways and other heavily utilized microhabitats (after Babcock, 1986). Traps were baited with carrots, shielded from exposure to sun, wind, and rain, and checked every 4 to 6 hours. Trapped animals were transported to a base camp for processing.

Individuals were anaesthetized immediately and kept at a moderate depth of anaesthesia with methoxyflurane (Metofane[TM]). Sex, weight, total length, and approximate age were determined on all captured animals. This information served to characterize factors that might modulate contaminant bioaccumulation. For individuals sampled destructively, liver tissue was extracted and weighed. Liver somatic index (LSI) was calculated as (liver wt/(total wt - liver wt)).

Lipid reserves were used as a parameter for evaluating intermediary fat metabolism and as an overall health indicator. Total fat content was determined using a commercial fat analyzer (EM-SCAN Model SA-2), composed of an insulated holding chamber wrapped with an electrically conductive coil. This instrument nondestructively measures the total electrical conductivity of the animal, which can be converted to lean body mass (Walsberg, 1988). The difference between the total body weight and lean body mass represents the total lipid content. The instrument was calibrated using 20 laboratory-reared ground squirrels for which whole body fat content was also determined by Soxhlet extraction following the methods of Bligh and Dyer (1959).

Nondestructive liver samples were obtained by pinch biopsy (as described by Slatter, 1985). A portion of the abdominal area was shaved and scrubbed with iodine and alcohol prior to biopsy. Fat samples were collected from the abdominal and/or gonadal region. To minimize the threat of predation, nondestructively sampled animals were placed in a trap and allowed to recover fully from the anesthesia (~12 hr) before being released at the location of capture. Numbered metal tags were attached to individuals' ears to identify them in subsequent sampling years.

Liver samples were weighed, divided for organic and inorganic analysis, and transferred to pre-cleaned I-Chem[TM] jars and acid-cleaned borosilicate vials with teflon screw-tops respectively. All fat and liver (whole and biopsy) samples were frozen (or nearly frozen) on site and shipped by air to the respective laboratories (OCs: Geochemical and Environmental Research Group at Texas A&M University: metals: Battelle Pacific Northwest).

Contaminant Analysis

Methods for heavy metal analysis have been previously reported in Allen-Gil et al. (1997). Freeze-dried samples (500 mg) were analyzed for arsenic (As). cadmium (Cd). copper (Cu), lead (Pb), and zinc (Zn) by inductively coupled plasma spectrometry (ICP-MS), for mercury (Hg) by cold vapor atomic absorption (CVAA), and for selenium (Se) and nickel (Ni) by either ICP-MS or graphite furnace atomic absorption (GFAA).

Tissue OC analysis was performed by the Geochemical and Environmental Research Group at Texas A&M University. The methods and quality assurance procedures have been reported in Allen-Gil et al. (in press). The procedures for liver and fat samples were adapted from those employed for the U.S. National Oceanic and Atmospheric Administration's Status and Trends Program and the USEPA's Environmental Monitoring-and Assessment Program (Wade et al., 1988, 1993; Sericano et al., 1990). These procedures were modified by adding 10x lower surrogate concentrations and injecting 10x less volume during gas chromatography to provide the lower method detection limits (MDLs) required for arctic samples. Briefly, tissues (0.5 - 15 g wet wt.) were extracted with C[H.sub.2][Cl.sub.2], fractionated using alumina:silica open column chromatography, purified by HPLC, and analyzed using dual column fused-silica capillary column gas chromatography with an electron capture detector (GC-ECD) using a Hewlett-Packard 5880A GC in the splitless mode.

Statistical Analysis

All contaminant data were [log.sub.10]-transformed as preliminary data exploration revealed proportional relationships between means and standard deviations for some analytes. As recommended by Hebert and Keenleyside (1995), data were not normalized for lipid (or percent moisture for metals) because preliminary data analysis did not support a strong or consistent correlation between percent lipid and the most frequently detected analytes ([r.sub.s]<0.50). After equal variance assumption validation using the modified Levine test, site and sex differences were examined by one-way ANOVA, followed by the Neuman-Keuls post-hoc multiple comparison test (software: NCSS, Kaysville, Utah). A significance level of 0.05 was applied.

Frequency of detection data was based only on data that passed the quality assurance (QA) test, and occurred above the MDL, which varied from sample to sample because of varying initial wet weights. There were numerous occasions in which an analyte was detected in a sample below the MDL. Calculations of concentration data include those samples in which the analyte was detected below the MDL, but do not include samples for which the analyte was not detected. As high variability in analyte concentrations has been observed in field studies, outliers were considered to represent variability among individuals and were therefore not eliminated.

RESULTS

Squirrels were trapped and sampled from all sites over the three-year study period. Characteristics of the sampled populations are presented in Table 1. Squirrels were collected after the breeding and parturition season, and sampled individuals were restricted to adults and subadults (> 400 g). Among general health parameters, only percent lipid in fat and liver somatic index showed site-related differences.
TABLE 1. Characteristics of arctic ground squirrels sampled from
sites in northern Alaska.

                         Elusive                  Schrader

                     9-11 August, 1991       14-18 August, 1991
Dates sampled       14-21 August, 1993     22 July-1 August, 1992

Total number               13                      26
  sampled:
  males/females           6/7                    12/14
Length (cm)       37.1 [+ or -] 2.6 (1)    38.3 [+ or -] 2.8
Weight (g)         599 [+ or -] 127         603 [+ or -] 141
Percent body
  weight
  as fat          19.4 [+ or -] 10.3       14.4 [+ or -] 10.8
Percent lipid
  in liver        2.59 [+ or -] 0.84       2.24 [+ or -] 1.31
Percent lipid
  in fat          76.9 [+ or -] 7.90 (a)   41.2 [+ or -] 10.6 (b)
Percent dry
  weight
  in liver        30.4 [+ or -] 1.4        38.5 [+ or -] 12.8
Percent dry
  weight
  in fat            96.5 [+ or -] 1.58     54.0 [+ or -] 15.0
Liver somatic
  index            3.0 [+ or -] 0.4 (a)    0.86 [+ or -] 0.98 (b)

                        Feniak

                    5-6 July, 1992
Dates sampled      6-10 August, 1993

Total number              13
  sampled:
  males/females          6/7
Length (cm)       36.8 [+ or -] 2.0
Weight (g)         593 [+ or -] 133
Percent body
  weight
  as fat          13.9 [+ or -] 10.5
Percent lipid
  in liver        2.46 [+ or -] 0.95
Percent lipid
  in fat          30.1 [+ or -] 24.9 (b)
Percent dry
  weight
  in liver        30.8 [+ or -] 7.8
Percent dry
  weight
  in fat          44.9 [+ or -] 25.9
Liver somatic
  index           2.92 [+ or -] 1.36 (a)

(1) Values are presented as arithmetic mean [+ or -]
standard deviation.

(a),(b) different letters indicate site differences
detected by one-way ANOVA.


Contaminant Burdens in Liver and Fat Tissue

Heavy metals: Concentrations of nonessential metals ranged from below detection to 32 [micro]g/g wet weight, with average concentrations below 0.5 [micro]g/g wet wt. (Table 2). The rank concentrations of metals was Zn > Cu > Cd > Se> As > Ni, Pb > Hg. Only a very small percentage of the mercury was present as methyl-Hg, typically less than 0.5%. Site differences were observed for Hg, Ni. and Pb, but patterns were not consistent among metals. Hg was higher in squirrels from Feniak Lake than Elusive Lake. Ni was higher in squirrels from Feniak and Elusive Lakes than in those from the Schrader Lake vicinity. Pb was higher in Feniak and Schrader squirrels than in those collected at Elusive Lake. Cd, Cu, and Hg concentrations increased with squirrel length (Table 3), but only Cd increased with weight. A negative correlation was observed between Se and weight. LSI was positively correlated with Ni and Se, but negatively correlated with Pb. There were no significant correlations between metals and percent body weight as fat. Metals tended to increase in concert with one another, as evidenced by the positive correlations between As and Cd, Cd and Cu, Cu and Zn, and Hg and Pb (Table 3).

Organochlorines in liver: HCB, trans-nonachlor, p,p'-DDE and PCBs 138 and 170 were most frequently detected in arctic ground squirrel livers (Table 4). These analytes were present in squirrels from all three sites. Compounds that were found infrequently included [gamma]-,[alpha]-, and oxy-chlordane, endrin, mirex, 1,2,3,4- and 1,2,4,5-tetrachlorobenzene (TCB), pentachlorobenzene, p,p'-DDT, p,p'-DDD, and PCBs 8, 52, 87, 153, and 180. The following analytes were not detected above the MDL in any squirrel liver samples: [alpha]-HCH, [beta]-HCH, [delta]-HCH, heptachlor, aldrin, endosulfan 2, pentachloroanisole, and o,p'-DDE, o,p'-DDD, o,p'-DDT and PCBs 29, 44, and 200. Greater than 85% of [SIGMA]DDTs was found as p,p'-DDE in most liver samples.

Consistent differences among sites or years of sampling for major analytes were not apparent. In liver, p,p'-DDE was the only OC showing a site effect (Schrader > Elusive and Feniak). PCBs were most often detected in Feniak squirrels, and the suite of PCB congeners found in squirrels from Schrader was reduced relative to the other two sites. PCBs 66, 101, 128, 153, 195, and 209 were not detected in squirrel livers from the Schrader site.

Among the most frequently detected analytes, there were no sex-related differences in OC concentrations. Although correlations between concentrations of OCs and squirrel weight were also not significant, negative correlations were observed between the percentage of body weight as fat and p,p'-DDE, trans-nonachlor, and PCBs 138 and 170 (see Table 3). PCBs 138, 170, and 180 increased in concert with one another.
TABLE 3. Significant Spearman correlation coefficients among
health parameters and liver contaminant concentrations.

Variable 1          Variable 2          Coefficient   N

Weight              Total Length            0.74      43
Weight              LSI                    -0.38      30
Total Length        % body wt. as fat       0.56      38
Total Length        % lipid in liver        0.35      40
% body wt. as fat   % lipid in liver        0.46      35

Weight              Cd                      0.55      42
Weight              Se                     -0.68       9

Total Length        Cd                      0.42      42
Total Length        Cu                      0.33      42
Total Length        Hg                      0.63      11

LSI                 Ni                      0.48      30
LSI                 Pb                     -0.48      30
LSI                 Se                      0.80       9
LSI                 t-nonachlor            -0.53      18
LSI                 p,p'-DDE               -0.50      21
LSI                 PCB 170                -0.70      18
LSI                 PCB 138                -0.64      25

% body wt. as fat   t-nonachlor            -0.53      26
% body wt. as fat   p,p'-DDE               -0.41      31
% body wt. as fat   PCB 170                -0.58      18
% body wt. as fat   PCB 138                -0.44      24

As                  Cd                      0.33      42
Cd                  Cu                      0.35      42
Cu                  Zn                      0.46      42
Hg                  Pb                      0.80      11
Ni                  p,p'-DDE               -0.37      32
Ni                  PCB 180                 0.85       8
Pb                  HCB                     0.50      29
Pb                  p,p'-DDE                0.35      33
Zn                  HCB                     0.46      29
Zn                  PCB 153                -0.94       6
PCB 170             PCB 138                 0.94      15
PCB 180             PCB 138                 0.83       6


Organochlorines in Fat: HCB, p,p'-DDE, and PCBs 138 and 153 were most frequently found in squirrel fat samples (Table 5). Unfortunately, fat samples from Elusive Lake squirrels rarely met the QA criteria for reporting. Between 71% and 100% of [SIGMA]HCHs was present as [alpha]-HCH in squirrel fat samples in which [alpha]-HCH was detected. Likewise, p,p'-DDE accounted for more than 90% of [SIGMA]DDTs in 6 of 13 squirrel fat samples in which this isomer was detected. The following analytes were not detected above the MDL in any fat samples: [gamma]-, [beta]-,and [delta]-HCH, heptachlor, aldrin, endosulfan 2, pentachloroanisole, and o,p'-DDE, o,p'-DDD, and o,p'-DDT. Total PCBs in fat was negatively correlated with squirrel weight ([r.sub.s] = -0.65, p < 0.01, n = 18). This relationship was largely driven by the more chlorinated congeners (PCBs 153 and 180).
TABLE 5. Organochlorine concentrations in arctic ground
squirrel fat ([micro]g/g wet weight).

Analyte              Site       N    Mean   SD

HCB                  Elusive     0
                     Feniak      8    2.0    2.1
                     Schrader    5    6.5    2.5

[alpha]HCH           Elusive     0
                     Feniak      9    1.0    1.1
                     Schrader    5    1.6    1.0

[gamma]HCH           all        13   n.d.

dieldrin             Elusive     0
                     Feniak      8    0.0    0.1
                     Schrader    5    0.5    0.8

endosulfan-2         Elusive     2    0.1    0.2
                     Feniak     10   n.d.
                     Schrader    5   n.d.

heptachlor epoxide   Elusive     0
                     Feniak      8    0.3    0.2
                     Schrader    5    0.6    0.5

trans-nonachlor      Elusive     2    0.1    0.2
                     Feniak     11    0.5    0.5
                     Schrader    5    0.6    0.5

p,p'-DDE             Elusive     0
                     Feniak      8    3.2    3.7
                     Schrader    5    7.9    3.9

[SIGMA]DDTs (1)      Elusive     0
                     Feniak      1    5.3
                     Schrader    0

[SIGMA]HCHs (2)      Elusive     0
                     Feniak      8    1.1    1.1
                     Schrader    5    1.6    1.0

PCB 8                all        14   n.d.
PCB 18               all        18   n.d.
PCB 28               all        18   n.d.
PCB 29               all        18   n.d.
PCB 44               all        18   n.d.
PCB 52               all        18   n.d.
PCB 66               all        13   n.d.

PCB 87               Elusive     1    0.1
                     Feniak      0   n.d.
                     Schrader    0   n.d.

PCB 101              all        18   n.d.

PCB 105              Elusive     1    0.2
                     Feniak      2    2.4    2.7
                     Schrader    5   n.d.

PCB 118              Elusive     1    0.5
                     Feniak      3    5.0    6.9
                     Schrader    0   n.d.

PCB 128              Elusive     1    0.2
                     Feniak      2    1.3    0.4
                     Schrader    5   n.d.

PCB 138              Elusive     2    0.4    0.1
                     Feniak     10    4.2    7.5
                     Schrader    5    0.5    0.4

PCB 153              Elusive     2    0.5    0.1
                     Feniak     10   13.6   24.3
                     Schrader    2    1.3    0.1

PCB 170              Elusive     1    0.2
                     Feniak      2    6.8    7.3
                     Schrader    0   n.d.

PCB 180              Elusive     2    0.3    0.3
                     Feniak     11    9.0    9.4
                     Schrader    4    0.6    0.3

PCB 187              Elusive     1    0.1
                     Feniak      2    0.4    0.0
                     Schrader    1    0.1

PCB 195              Elusive     0
                     Feniak      1    1.9
                     Schrader    5   n.d.

PCB 200              all        18   n.d.

PCB 206              Elusive     1    0.1
                     Feniak      4    1.1    1.4
                     Schrader    5   n.d.

PCB 209              Elusive     0   n.d.
                     Feniak      2    0.4    0.2
                     Schrader    5   n.d.

Analyte              Site       Minimum   Maximum

HCB                  Elusive
                     Feniak      <mdl       5.1
                     Schrader     4.6      10.9

[alpha]HCH           Elusive
                     Feniak      <mdl       3.0
                     Schrader    <mdl       2.8

[gamma]HCH           all

dieldrin             Elusive
                     Feniak      <mdl       0.3
                     Schrader    <mdl       1.8

endosulfan-2         Elusive     <mdl       0.3
                     Feniak
                     Schrader

heptachlor epoxide   Elusive
                     Feniak      <mdl       0.5
                     Schrader    <mdl       1.3

trans-nonachlor      Elusive     <mdl       0.3
                     Feniak      <mdl       1.3
                     Schrader    <mdl       1.4

p,p'-DDE             Elusive
                     Feniak      <mdl       9.4
                     Schrader     3.3      13.5

[SIGMA]DDTs (1)      Elusive
                     Feniak
                     Schrader

[SIGMA]HCHs (2)      Elusive
                     Feniak      <mdl       3.0
                     Schrader    <mdl       2.8

PCB 8                all
PCB 18               all
PCB 28               all
PCB 29               all
PCB 44               all
PCB 52               all
PCB 66               all

PCB 87               Elusive
                     Feniak
                     Schrader

PCB 101              all

PCB 105              Elusive
                     Feniak       0.5       4.3
                     Schrader

PCB 118              Elusive
                     Feniak       0.7      12.9
                     Schrader

PCB 128              Elusive
                     Feniak       1.1       1.6
                     Schrader

PCB 138              Elusive      0.4       0.5
                     Feniak       0.0      18.4
                     Schrader     0.3       1.1

PCB 153              Elusive      0.4       0.6
                     Feniak       0.4      62.6
                     Schrader     1.3       1.4

PCB 170              Elusive
                     Feniak       1.7      12.0
                     Schrader

PCB 180              Elusive      0.2       0.5
                     Feniak      15.5       0.2
                     Schrader     0.2       0.9

PCB 187              Elusive
                     Feniak       0.3       0.4
                     Schrader

PCB 195              Elusive
                     Feniak
                     Schrader

PCB 200              all

PCB 206              Elusive
                     Feniak       0.1       3.0
                     Schrader

PCB 209              Elusive
                     Feniak       0.3       0.5
                     Schrader

Concentration values include all samples in which analyte was
detected, using analytical estimates for samples less than the
method detection limit.

n.d. = not detected.

< mdl = less than method detection limit.

(1) [SIGMA]DDTs = p,p'-DDE, p,p'-DDD. p,p'-DDT.

(2) [SIGMA]HCHs = [alpha]HCH + [gamma]HCH.


DISCUSSION

Our results indicate a low level of heavy metal accumulation in arctic ground squirrels, similar to that reported for other North American arctic terrestrial herbivores. In caribou, lemming, and ptarmigan livers from the Canadian High Arctic, nickel was not detectable in all species, and lead concentrations were not detectable in ptarmigan and were 1.0 and 3.5 [micro]g/g wet wt. or lower in lemming and caribou respectively (Shaw and Gunn, 1981). Livers of caribou from the eastern Canadian Arctic had similar concentrations of Ni, Pb, and Hg, but Cd concentrations five times higher than those we observed in ground squirrels (Elkin and Bethke, 1995). We suspect that the higher level of Cd in caribou reflects differences in age and concentrations of liver metal-binding proteins (metallothioneins) between caribou and squirrels. In polar bears, Cd and Hg concentrations in livers from Svalbard were also within the range observed in ground squirrels (Norheim et al., 1992), while four bears from the Canadian High Arctic had Hg concentrations in liver in excess of 100 [micro]g/g wet wt. (Norstrom et al., 1986). Although Hg and other heavy metals can be atmospherically transported, deposition zones are usually not extensive (Stickel, 1973; Landers et al., in press). Local and regional areas of elevated heavy metal contamination in arctic fauna are more likely related to mineral-rich geologic areas (Norstrom et al., 1986; Allen-Gil et al., 1997).

The occurrence of OCs in a herbivorous rodent from remote areas of northern Alaska highlights the spatial and temporal pervasiveness of OC contamination. This finding supports the global distillation model developed by Wania and Mackay (1993, 1995, 1996), and empirical data for terrestrial (Simonich and Hites, 1995) and freshwater ecosystems (Muir et al., 1995; Allen-Gil et al., 1997). While the magnitude of contamination in arctic ground squirrels is not high relative to other areas and species, it represents an important source for food chain transfer and potential biomagnification (Larsson et al., 1990a).

Concentrations of OCs in ground squirrels from northern Alaska are not elevated relative to those in herbivorous small mammals from other areas or in other arctic wildlife species. In a review of arctic terrestrial contamination, Thomas et al. (1992) reported concentrations of OCs in caribou, hare. ptarmigan, and musk-ox from the Canadian Arctic. For [SIGMA]DDTs and [SIGMA]PCBs, concentrations in arctic herbivores throughout North America are typically below 50 ng/g wet wt. and 100 ng/g wet wt. respectively. Concentrations of OC pesticide in arctic ground squirrels were in the same range as those reported for carcass samples from rock ptarmigan (Lagopus mutus), a common herbivorous arctic ground bird (< 10 ng/g wet wt. for individual analytes, according to Snyder-Conn and Lubinski, 1993). Maximum concentrations of persistent organic contaminants in arctic ground squirrel fat were lower than approximate mean values in Canadian caribou fat (HCB = 26 ng/g wet wt., [SIGMA]HCH=20, [SIGMA]PCBs = 16, according to Elkin and Bethe, 1995). Reindeer liver from northern Sweden were also found to contain less than 1 ng/g wet wt. of most OCs, with the exception of PCB 153, which occurred at concentrations of 20 ng/g in some samples (Villeneuve et al., 1985).

In addition to predicted species differences in OC accumulation based on food web position and percent body weight as fat, geographic differences have also been observed. In polar bears, OC tissue concentrations decreased with increasing latitude and from east to west (Norstrom et al., 1988). The same pattern was observed in sediment cores for mercury, an atmospherically transported heavy metal (Lockhart et al., 1995).

Maximum [SIGMA]DDTs in arctic ground squirrel fat and liver were 40 ng/g wet wt., compared to mean total body residues of [SIGMA]DDTs in mice and voles from reference sites in Maine of 30 ng/g wet wt. (Dimond and Sherburne, 1969). Maximum [SIGMA]PCBs in arctic ground squirrel livers were 50 ng/g wet wt., compared to 1300 ng/g wet wt. in small mammal livers from an uncontaminated site in South Dakota (Greichus and Dohman, 1980).

Although the number of analyzed samples is too low to make definitive statements, it appears that OC pesticide and PCB residues in arctic herbivores are typically one to two orders of magnitude lower than values reported for arctic predators and marine mammals. For example, maximum [SIGMA]PCBs in arctic ground squirrel liver was 4.3 [micro]g/g lipid, compared to 12.5 [micro]g/g lipid in the livers of Svalbard fox (Norheim, 1978). Ringed seals, beluga whales, and polar bears sampled in Arctic regions frequently have contaminant burdens that are a hundred times higher than those observed in arctic ground squirrels (Bowes and Jonkel, 1975; Muir et al., 1988; Norstrom et al., 1988; Oehme et al., 1988; Norheim et al., 1992; Thomas et al., 1992; Cameron and Weis, 1993).

The negative correlations between tissue OC concentrations and body fat that we observed in squirrels likely reflect several processes. First, as the mass of body fat increases, a larger volume of tissue is available for OC deposition (Leatherland et al., 1979; Kawai et al., 1988). Second, shifting dietary habits may result in concurrent, but unassociated changes in OC uptake and eliminations, as well as body fat content. A third possibility is that OC burdens altered lipid metabolism in squirrels. Laboratory studies with fish have shown a decrease in carcass lipid following PCB exposure (Leatherland and Sonstegard, 1979; Leatherland et al., 1979). A fourth possibility is that these results are an artifact of correlation analysis on multivariate data sets, for which distinguishing between ecologically meaningful and spurious relationships is not always possible.

The lack of sex-related differences in OC concentrations in ground squirrels differs from results for fish and marine mammal species (Norheim et al., 1992; Sjim et al., 1992; Larsson et al., 1993). This difference is probably explained by the more similar pattern of fat deposition and utilization between the sexes in ground squirrels relative to nonhibernating species. In squirrels, both males and females have dramatic annual fluctuations in fat reserves: males increase their percent body weight as fat from 11% to 44% and females from 25% to 61% over the course of the summer (Batzli and Sobaski, 1980). Weight loss during hibernation is slightly higher for females than for males (8-22% versus 25-32%), presumably because females tend to hibernate longer than males (McLean and Towns, 1981).

CONCLUSION

This study documents the occurrence of heavy metals and anthropogenically derived OC contaminants in remote regions of the U.S. Arctic. Heavy metal accumulation in arctic ground squirrels from Alaska is not elevated relative to other species and arctic locations, and probably reflects the minerally rich geology of northern Alaska. The fact that detectable levels of HCB, HCHs, chlordanes, DDTs and PCBs were found in a small terrestrial herbivore with a limited home range size from several sites illustrates the pervasiveness of these compounds in the global environment. Although contamination in ground squirrels is not high relative to small herbivorous mammals in the contiguous U.S. or other wildlife species in the Arctic, there may be some cause for concern and further study regarding the possibility of sublethal toxicity and biomagnification.
TABLE 2. Heavy metal concentrations in arctic ground
squirrel liver ([micro]g/g wet weight).

Analyte                  Site       *   N    Mean

Arsenic                  Elusive        13    0.18
                         Feniak         13    0.08
                         Schrader       23    0.11

Cadmium                  Elusive        13    0.37
                         Feniak         13    0.16
                         Schrader       23    0.65

Copper                   Elusive        13    5.99
                         Feniak         13    5.95
                         Schrader       23    6.03

Total Mercury            Elusive    a    7    0.02
                         Feniak     b    8    0.05
                         Schrader        0

% Mercury as methyl-Hg   Elusive         3    0.37
                         Feniak          7    0.13
                         Schrader        0

Nickel                   Elusive    a   13    0.15
                         Feniak     a   13    0.09
                         Schrader   b   23    0.03

Lead                     Elusive    a   13    0.03
                         Feniak     b   13    0.18
                         Schrader   b   23    0.13

Selenium                 Elusive         7    0.26
                         Feniak          5    0.23
                         Schrader        0

Zinc                     Elusive        13   32.60
                         Feniak         13   33.26
                         Schrader       23   35.19

Analyte                  Site        SD    Min.    Max.

Arsenic                  Elusive    0.27    0.03    1.02
                         Feniak     0.08    0.03    0.30
                         Schrader   0.10    0.01    0.35

Cadmium                  Elusive    0.49    0.05    1.74
                         Feniak     0.17    0.02    0.60
                         Schrader   1.01    0.03    4.78

Copper                   Elusive    0.68    4.86    7.50
                         Feniak     1.07    4.08    7.85
                         Schrader   1.30    4.12    8.35

Total Mercury            Elusive    0.02    0.01    0.06
                         Feniak     0.02    0.02    0.08
                         Schrader

% Mercury as methyl-Hg   Elusive    0.07    0.30    0.43
                         Feniak     0.05    0.06    0.20
                         Schrader

Nickel                   Elusive    0.39    0.01    1.45
                         Feniak     0.14    0.03    0.55
                         Schrader   0.03    0.00    0.13

Lead                     Elusive    0.02    0.01    0.07
                         Feniak     0.22    0.01    0.83
                         Schrader   0.08    0.02    0.28

Selenium                 Elusive    0.21    0.09    0.56
                         Feniak     0.06    0.17    0.32
                         Schrader

Zinc                     Elusive    3.83   26.85   38.20
                         Feniak     7.85   22.20   50.09
                         Schrader   8.61   24.75   61.38

Concentration values include all samples in which analyte was
detected, using analytical estimates for samples less than the
method detection limit.

* different letters indicate site differences detected by
one-way ANOVA.
TABLE 4. Organochlorine concentrations in arctic ground
squirrel liver ([micro]g/g wet weight).

Analyte                 Site       *   N    Mean     SD

HCB                     Elusive        11    0.24    0.22
                        Feniak          9    0.48    0.31
                        Schrader       12    0.41    0.21

[alpha]-HCH             all             0

[gamma]-HCH             Elusive         4    1.36    0.61
                        Feniak          0
                        Schrader        2    1.85    2.13

dieldrin                Elusive         7   10.91   12.46
                        Feniak          7    1.53    1.68
                        Schrader        7   14.42   25.55

endosulfan-2            all             0

heptachlor epoxide      Elusive         0
                        Feniak          0
                        Schrader        4    2.80    1.67

trans-nonachlor         Elusive         9    0.87    1.28
                        Feniak          7    1.42    0.67
                        Schrader       13    3.43    4.34

p,p'-DDE                Elusive    a   13    1.51    1.56
                        Feniak     a    6    0.86    1.11
                        Schrader   b   17    4.47    4.75

[SIGMA]DDTs (1)         Elusive        13    6.13    9.17
                        Feniak          6    1.43    1.93
                        Schrader       17   12.25   12.14

[SIGMA]HCHs (2)         Elusive         4    1.36    0.61
                        Feniak          0
                        Schrader        2    1.85    2.13

[SIGMA]chlordanes (3)   Elusive         2    0.25    0.08
                        Feniak          1    1.12
                        Schrader        9    4.28    6.38

PCB 8                   Elusive         1    3.57
                        Feniak          4   18.19   21.48
                        Schrader        2    0.48    0.01

PCB 18                  Elusive         0
                        Feniak          1    0.19
                        Schrader        2    1.16    0.94

PCB 28                  Elusive         2    0.28    0.15
                        Feniak          0
                        Schrader        3    0.56    0.65

PCB 29                  all             0

PCB 44                  all             0

PCB 52                  Elusive         3    0.71    0.50
                        Feniak          6    0.65    0.39
                        Schrader        3    0.20    0.01

PCB 66                  Elusive         2    1.56    0.56
                        Feniak          1    0.49
                        Schrader        0

PCB 87                  Elusive         5    0.05    0.02
                        Feniak          2    1.71    2.28
                        Schrader        2    3.09    3.81

PCB 101                 Elusive         3    0.22    0.16
                        Feniak          2    0.19    0.01
                        Schrader        0

PCB 105                 Elusive         3    0.08    0.09
                        Feniak          2    0.41    0.16
                        Schrader        0

PCB 118                 Elusive         3    0.17    0.16
                        Feniak          2    1.20    0.88
                        Schrader        0

PCB 128                 Elusive         2    0.10    0.06
                        Feniak          1    0.11
                        Schrader        0

PCB 138                 Elusive         4    0.48    0.10
                        Feniak         10    1.45    0.95
                        Schrader       16    3.53    3.84

PCB 153                 Elusive         4    0.85    0.17
                        Feniak          4    1.96    2.50
                        Schrader        0

PCB 170                 Elusive         4    0.52    0.16
                        Feniak          6    1.06    0.89
                        Schrader       16    3.53    3.84

PCB 180                 Elusive         2    0.34    0.27
                        Feniak          4    1.27    1.53
                        Schrader        2    0.13    0.07

PCB 187                 Elusive         3    0.19    0.03
                        Feniak          2    0.17    0.03
                        Schrader        1    0.14

PCB 195                 Elusive         1    0.16
                        Feniak          1    0.11
                        Schrader        0

PCB 200                 all             0

PCB 206                 Elusive         1    0.05
                        Feniak          0
                        Schrader        0

PCB 209                 Elusive         1    0.11
                        Feniak          1    0.09
                        Schrader        0

[SIGMA]PCBs (4)         Elusive         1    2.09
                        Feniak         11    9.72   14.31
                        Schrader       10    5.72    4.70

Analyte                 Site       Minimum   Maximum

HCB                     Elusive     0.05       0.82
                        Feniak      0.17       0.95
                        Schrader    0.15       0.96

[alpha]-HCH             all

[gamma]-HCH             Elusive     0.68       1.96
                        Feniak
                        Schrader    0.35       3.36

dieldrin                Elusive     0.74      28.70
                        Feniak      0.22       4.90
                        Schrader    0.51      71.04

endosulfan-2            all

heptachlor epoxide      Elusive
                        Feniak
                        Schrader    0.54       4.42

trans-nonachlor         Elusive     0.15       4.16
                        Feniak      0.78       2.76
                        Schrader    0.08      15.55

p,p'-DDE                Elusive     0.33       5.57
                        Feniak      0.19       3.10
                        Schrader    0.12      13.63

[SIGMA]DDTs (1)         Elusive     0.34      34.08
                        Feniak      0.19       5.16
                        Schrader    0.12      39.76

[SIGMA]HCHs (2)         Elusive     0.68       1.96
                        Feniak
                        Schrader    0.35       3.36

[SIGMA]chlordanes (3)   Elusive     0.19       0.30
                        Feniak
                        Schrader    0.08      19.96

PCB 8                   Elusive     3.57       3.57
                        Feniak      0.51      48.69
                        Schrader    0.47       0.49

PCB 18                  Elusive
                        Feniak      0.19       0.19
                        Schrader    0.49       1.82

PCB 28                  Elusive     0.17       0.39
                        Feniak
                        Schrader    0.07       1.30

PCB 29                  all

PCB 44                  all

PCB 52                  Elusive     0.16       1.14
                        Feniak      0.27       1.35
                        Schrader    0.20       0.21

PCB 66                  Elusive     1.16       1.95
                        Feniak      0.49       0.49
                        Schrader

PCB 87                  Elusive     0.03       0.07
                        Feniak      0.10       3.33
                        Schrader    0.40       5.79

PCB 101                 Elusive     0.05       0.38
                        Feniak      0.18       0.20
                        Schrader

PCB 105                 Elusive     0.01       0.18
                        Feniak      0.30       0.53
                        Schrader

PCB 118                 Elusive     0.06       0.35
                        Feniak      0.58       1.83
                        Schrader

PCB 128                 Elusive     0.06       0.14
                        Feniak
                        Schrader

PCB 138                 Elusive     0.39       0.62
                        Feniak      0.29       2.96
                        Schrader    0.09      12.25

PCB 153                 Elusive     0.66       1.02
                        Feniak      0.21       5.62
                        Schrader

PCB 170                 Elusive     0.36       0.68
                        Feniak      0.44       2.83
                        Schrader    0.09      12.25

PCB 180                 Elusive     0.15       0.53
                        Feniak      0.25       3.54
                        Schrader    0.08       0.18

PCB 187                 Elusive     0.17       0.23
                        Feniak      0.15       0.19
                        Schrader    0.14       0.14

PCB 195                 Elusive
                        Feniak
                        Schrader

PCB 200                 all

PCB 206                 Elusive     0.05       0.05
                        Feniak
                        Schrader

PCB 209                 Elusive     0.11       0.11
                        Feniak      0.09       0.09
                        Schrader

[SIGMA]PCBs (4)         Elusive     2.09       2.09
                        Feniak      1.47      50.04
                        Schrader    0.74      12.74

Concentration values include all samples in which analyte was
detected, using analytical estimates for samples less than the
method detection limit.

* different letters indicate site differences detected by
one-way ANOVA.

(1) [SIGMA]DDTs = p,p'-DDE, p,p'-DDD, p,p'-DDT.

(2) [SIGMA]HCHs = [alpha]HCH + [gamma]HCH.

(3) [SIGMA]chlordanes = [alpha]chlordane + [gamma]chlordane
+ trans-nonachlor + heptachlor epoxide.

(4) [SIGMA]PCBs = sum of congeners: 8, 18, 28, 29, 44, 52, 66,
87, 101, 105, 118, 128, 138, 153, 170, 187, 195, 200, 206, 209.


ACKNOWLEDGEMENTS

This research was funded by the U.S. Environmental Protection Agency through cooperative agreements with Oregon State University (CR 818187), Battelle Pacific Northwest (CR 820871) and the Geochemical and Environmental Research Group at Texas A&M University (CR 820767). It has been subjected to the Agency' s peer and administrative review and approved for publication. This manuscript is Oregon State University, Agricultural Experiment Station Technical Paper No. 11065. Mention of trade names of commercial products does not constitute endorsement or recommendation for use.

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S.M. ALLEN-GIL, (1) D.H. LANDERS, (2) T.L. WADE, (3) J.L. SERICANO, (3) B.K. LASORSA, (4) E.A. CRECELIUS (4) and L.R. CURTIS (5)

(1) Department of Fisheries and Wildlife, 104 Nash Hall, Oregon State University, Corvallis, Oregon 97331, U.S.A.; present address: National Research Council Associate, U.S. EPA National Health and Environmental Effects Research Laboratory, 200 SW 35th St., Corvallis, Oregon 97333, U.S.A.; allens@mail.cor.epa.gov

(2) U.S. EPA National Health and Environmental Effects Research Laboratory, 200 SW 35th St., Corvallis, Oregon 97333, U.S.A.

(3) Geochemical and Environmental Research Group, Texas A&M University, 833 Graham Road, College Station, Texas 77845, U.S.A.

(4) Battelle Pacific Northwest Division, 1529 West Sequim Bay Road, Sequim, Washington 98382, U.S.A.

(5) Department of Fisheries and Wildlife, 104 Nash Hall, Oregon State University, Corvallis, Oregon 97331, U.S.A.; present address: Department of Environmental Health, College of Public and Allied Health, East Tennessee State University, Johnson City, Tennessee 37614-0682, U.S.A.

RESUME. De 1991 a 1993, on a mesure les concentrations en metaux lourds et en organochlores, y compris des pesticides organochlores et des congeneres du diphenyle polychlore (PCB), chez le spermophile arctique (Spermophilus parryi) a trois endroits situes dans la chaine de Brooks de l'Alaska septentrional. On a trouve des metaux lourds dans la plupart des foies de spermophiles preleves, avec des concentrations en elements traces (As, Cd, Hg, Ni et Pb) inferieures en moyenne a [micro]g/g de poids frais. L'hexachlorobenzene (HCB), le p,p'-DDE, l'hexachlorocyclohexane gamma (HCH-[gamma]), le trans-nonachlore et les PCB 138, 153 et 170 etaient les organochlores les plus frequemment detectes dans le tissu adipeux et le foie. Les concentrations moyennes des organochlores analyses individuellement etaient inferieures a 20 ng/g de poids frais pour le foie et a 15 ng/g de poids frais pour le tissu adipeux. Les correlations de rang revelent que les concentrations en metaux lourds augmentent de concert avec celles en organochlores (As, Cd, Cu et Zn; PCB 138, 170 et 180). Bien que les concentrations en metaux lourds et en organochlores soient faibles par rapport a celles d'autres regions et a celles d'autres especes arctiques, la presence de ces composes illustre l'omnipresence planetaire de composes organiques persistants et le potentiel pour une accumulation biologique dans le reseau trophique terrestre de l'Arctique.

Mots cles: metaux lourds, pesticides organochlores, diphenyles polychlores, Spermophilus parryi, Alaska septentrional

Traduit pour la revue Arctic par Nesida Loyer.
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Author:S.M. Allen-Gil, and others
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Date:Dec 1, 1997
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