Environ. Sci. Technol. 2007, 41, 1494-1500
Arsenic Accumulation in Bark Beetles and Forest Birds Occupying Mountain Pine Beetle Infested Stands Treated with Monosodium Methanearsonate CHRISTY A. MORRISSEY,† COURTNEY A. ALBERT,‡ PATTI L. DODS,† WILLIAM R. CULLEN,§ VIVIAN W.-M. LAI,§ AND J O H N E . E L L I O T T * ,† Environment Canada, Canadian Wildlife Service, Pacific Wildlife Research Centre, 5421 Robertson Road, Delta, British Columbia, Canada, V4K 3N2, Department of Biological Sciences, Simon Fraser University, 8888 University Drive, Burnaby, British Columbia, Canada, V5A 1S6, and Chemistry Department, University of British Columbia, 2075 Westbrook Mall, Vancouver, British Columbia, Canada, V6T 1Z3
The arsenic-based pesticide, monosodium methanearsonate (MSMA), is presently being evaluated for re-registration in Canada and the United States and has been widely used in British Columbia to help suppress Mountain Pine Beetle (MPB) outbreaks. We assessed the availability and exposure of MSMA to woodpeckers and other forest birds that may prey directly on contaminated bark beetles. Total arsenic residues in MPB from MSMA treated trees ranged from 1.3-700.2 µg g-1 dw (geometric mean 42.0 µg g-1) with the metabolite monomethyl arsonic acid (MMAA) contributing 90-97% to the total arsenic extracted. Live adult and larval beetles were collected from treated trees and reached concentrations up to 327 µg g-1 dw. MPBs from reference trees had significantly lower arsenic concentrations averaging 0.19 µg g-1 dw. Woodpeckers foraged more heavily on MSMA trees that contained beetles with lower arsenic residues, suggesting those trees had reduced MSMA translocation and possibly greater live beetle broods. Blood samples from five species of woodpeckers and other forest passerines breeding within 1 km of MSMA stands contained elevated levels of total arsenic but with large individual variability (geometric mean ) 0.18 µg g-1 dw, range 0.02-2.20 µg g-1). The results indicate that there is significant accumulation and transfer of organic arsenic within the food chain at levels that may present a toxicity risk to avian wildlife.
Introduction The current outbreak of Mountain Pine Beetle (MPB) (Dendroctonus ponderosae Hopkins) in British Columbia (B.C.), Canada, is estimated to be the largest insect epidemic recorded in North American history, infesting an area over * Corresponding author phone: (604)940-4680; fax: 604 946-7022; e-mail:
[email protected]. † Pacific Wildlife Research Centre. ‡ Simon Fraser University. § University of British Columbia. 1494
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8.7 million hectares in 2005 (1, 2). Management strategies employ a variety of techniques to reduce timber losses from beetle outbreaks including the use of pesticides such as monosodium methanearsonate (MSMA). MSMA is an organic arsenical used in the United States for weed control on cotton crops, seed grasses, turf, nonbearing orchards, vineyards, recreational areas, and rights of way (3). In Canada, it has only been registered for use in the forest industry primarily to combat natural infestations of both MPB and Spruce Beetle (Dendroctonus rufipennis Kirby) and for tree thinning. Although several strategies have been applied for suppressing incipient beetle populations, MSMA was favored by foresters under certain conditions for its low cost and ease of use in remote areas where harvesting was not feasible (2). On the basis of estimates of reported usage for bark beetle control in B.C. during a 10-year period from 1995 to 2004, approximately 5080 kg of MSMA was applied amounting to almost 500 000 trees (4). The bioavailability, uptake, and toxicity of arsenic are dependent on chemical form and oxidation state of the compound, type of organism exposed, environmental conditions, and concentrations of phosphate and sulfate ions that are known to compete with arsenic (5). MSMA and other related organic arsenicals were generally considered to have low toxicity because the biomethylation of inorganic arsenic was deemed a detoxification process. For example, in mammals, dimethlylarsinic acid (DMAAV) has low acute toxicity and is readily excreted (6, 7). However, current knowledge of organic arsenic metabolism and toxicity indicates that a series of oxidation and reduction reactions of MSMA can produce intermediary trivalent methylated forms, particularly MMAAIII, which are more toxic than even inorganic arsenite (8-10). In addition, the trivalent forms of monomethyl arsonic acid (MMAAIII) and dimethyl arsinic acid (DMAAIII) both have direct genotoxic action (11) and DMAA has carcinogenic properties (12). Therefore, depending on the oxidation state, the methylation of arsenic is now recognized as a mechanism of toxicity rather than solely a detoxification process. As a result, MSMA is currently being re-evaluated for its future registration in both Canada and the United States (3, 13). The B.C. forest industry has been using MSMA for over 20 years and increasingly in response to the bark beetle problem. However, the movement of MSMA and its arsenic derivatives to nontarget wildlife was assumed negligible given the discrete nature of the application procedure, which targets beetle eggs and larvae under the tree bark. Although the toxicity of MSMA has been identified in several laboratory studies of select mammals and aquatic species (see summaries 3, 10, 14), there have been no studies conducted on wild insectivorous birds that potentially have direct oral exposure to MSMA. Woodpeckers and other forest birds such as chickadees and nuthatches are frequently attracted to beetle outbreak areas because of increased food availability, and several species have been shown to alter their diet in response to beetle outbreaks (15-17). Given the current MPB epidemic and the subsequent increased use of MSMA in many areas of British Columbia, we hypothesized that several bird species may be exposed to MSMA or its arsenic derivatives from consuming contaminated invertebrate prey. Therefore, this study aims to assess the availability and exposure of MSMA to insectivorous forest birds by investigating (1) beetle accumulation of MSMA metabolites, (2) beetle survivorship of MSMA treatment, and (3) evidence of birds consuming contaminated beetles from MSMA treated trees. 10.1021/es061967r CCC: $37.00
2007 American Chemical Society Published on Web 01/06/2007
Experimental Section Study Area. The study area was located in the Cascades Forest District primarily between Merritt and Princeton in the southern interior of British Columbia, Canada where MPB infestations are at epidemic levels and MSMA treatments have been frequently used in effort to contain or control further infestation. We targeted forest areas which received recent MSMA treatments (i.e., treated 1-2 years prior) using information provided by the B.C. Ministry of Forests and local timber harvesting operators. Selected MSMA stands had approximately 50-200 recently treated trees at the site. MSMA Application Procedure. Adult MPB attack live lodgepole pine (Pinus contorta) trees usually in mid to late July or early August and construct galleries and lay eggs which mature into larvae that overwinter, pupate, and emerge the following summer. Foliage color (green attack ) new infestation, red attack ) year following infestation, and gray attack ) 2 or more years post attack) and the presence of pitch tubes on the bole of the tree are routinely used to assess the stage of MPB attack. Application procedures for MSMA treatment of lodgepole pine infested with MPB follow a series of discrete steps designed specifically to target the beetle and to minimize the impact to surrounding environment. Beetles are targeted for treatment while in the egg or early larval stages within 2-3 weeks postattack to prevent emergence the following summer. Trees are often baited with semiochemicals to attract beetles, and the pesticide is applied by cutting an axe frill into the cambium near the base of the tree and squirting the MSMA into the frill at the prescribed rate of 1 mL of Glowon (United Agri Products Canada) (0.32 kg elemental As (as MSMA)/L water and additives) per 2.5 cm of tree circumference (18). The arsenic translocates through the xylem into the phloem resulting in death of the tree and direct and indirect toxicity to the beetles (19, 20). Typically, 10-100 trees are treated per site, and trees are not removed following treatment. Bark Beetle Collections. We assessed the potential threat to avian predators through arsenic analysis of adult and larval/ pupal MPB and other insects. Other insects sampled included predators of MPB (Clerid larvae), pine engravers (Ips adults), wood-boring beetles, and unidentified insects. Insects were collected from infested lodgepole pine trees treated with MSMA approximately 4 weeks (green attack) and almost 1 year (red attack) post-treatment (June-August). We removed the bark with an axe and collected individuals from beetle galleries with forceps and transferred them into clean glass jars. Additional samples were collected from nearby lodgepole pines that were also infested with MPB but were not treated with MSMA (reference trees). In the spring and summer of 2002, 17 insect samples were collected from both MSMA and reference trees that had evidence of woodpecker foraging activity (debarking index g 3). In 2003, 2004, and 2005, we collected 23, 19, and 29 samples, respectively, of MPB in the same manner but from trees with different levels of debarking (debarking index 0-7). The debarking index refers to visual inspection of the whole tree to assess the amount of bark removal which represents the extent of woodpecker foraging, where 0 ) no debarking, 1 ) 90%) were collected within 2 m above the axe frill where MSMA is applied. Each sample consisted of a composite of >10 individual beetles from a single tree. A few samples (n ) 3) with insufficient mass/ beetles for arsenic analysis were pooled with another similar sample collected at the same site/time and with similar characteristics (i.e., same debarking score, life stage).
Forest Bird Trapping. During the breeding seasons (April-July) of 2004 and 2005, Three-Toed (Picoides dorsalis) and Hairy woodpeckers (Picoides villosus) occupying territories typically within 1 linear km of recent MSMA stands (treated in previous 2 years) were targeted for capture to obtain blood samples. We concentrated on capturing individuals or pairs of these species, as bark beetles are reported to comprise a large proportion of their diets (16). In total, 23 birds (19 Hairy and 4 Three-Toed woodpeckers) were captured in mistnets using combinations of playback calls, dummy specimens, and suet feeders as attractants or in bag nets placed over the entrance of the nesting cavity. An additional nine Red-Naped sapsuckers (Sphyrapicus nuchalis) were captured using the same techniques. Woodpeckers were aged by feather molt patterns (21), were sexed, weighed, measured (tarsus, wing, tail, bill), and banded, and 0.5 mL of blood was taken by venipuncture of the jugular vein to use for total arsenic analysis. In 2005, we also captured two other forest bird species breeding near MSMA stands: 19 adult Mountain chickadees (Parus gambeli) and 2 adult RedBreasted nuthatches (Sitta canadensis). Chickadees and nuthatches were weighed, measured, and banded, and a 0.1mL sample of blood was taken by venipuncture of the jugular vein. All procedures for trapping and handling birds were in accordance with Animal Care and Federal scientific permits. Arsenic Analysis. All bark beetle and bird blood samples were analyzed for total arsenic. Bark beetles collected in 2002 and 2003 and a subsample in 2005 were further analyzed for organic and inorganic arsenic speciation. Sample preparation and analyses were performed in Dr. William Cullen’s laboratory at the University of British Columbia. Samples for total arsenic analysis were freeze-dried (0.020.2 g) and acid digested using nitric acid and hydrogen peroxide. Samples after digestion were diluted appropriately with the rhodium-nitric acid solution and were stored at 4 °C until analysis. Total arsenic analysis was performed using inductively coupled plasma mass spectroscopy (ICP-MS). Signals were corrected according to the signal of the internal rhodium standard. Quality assurance of total arsenic analysis was maintained by analyses of procedural blanks and at least two certified reference materials plus an in-house standard. Reference materials included dogfish muscle (Dorm-2) (certified value: 18.0 ( 1.1 µg As g-1 dw), dogfish liver (Dolt2) (certified value: 16.6 ( 1.1 µg As g-1 dw) (National Research Council, Canada), sea plant homogenate (IAEA Fucus) (certified value: 44.3 ( 2.2 µg As g-1 dw) (National Institute of Standards and Technology, U.S. Department of Commerce), and the house standard (Kelp powder) (reported value: 27.7 µg As g-1 dw). Analytical results were typically within 5% of these certified values (max range 96-113%). Reliable quantification of total arsenic in all samples (method detection limit) was between 0.02 and 0.03 µg g-1. Samples for speciation of arsenic were also freeze-dried (0.02-0.2 g dry mass) and extracted using a procedure similar to that previously described (22, 23). Extracts were stored at -20 °C and were transferred to the cold room (∼4 °C) on the day of analysis. Speciation of extracts was performed using high-performance liquid chromatography (HPLC) combined with an ICP-MS detector. Arsenic compounds in the samples were identified and quantified by matching the retention times of the peaks in the chromatograms with those of known standards. Speciation consisted of identifying inorganic arsenic, arsenate (AsV) and arsenite (AsIII), and major organic forms, monomethyl arsonic acid (MMAA), which is the deionized form of MSMA, and dimethyl arsinic acid (DMAA). It is technically difficult to distinguish between the oxidation states of organic arsenic using current analytical procedures. As a result, we could not identify the different valence states of the organic arsenicals (i.e., MMAAV and the more toxic form MMAAIII) and generically report MMAA and DMAA to VOL. 41, NO. 4, 2007 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 1. Summary of Total Arsenic Measured in 90 Composite Samples of Bark Beetles from MSMA Treated and Reference Trees in the Cascades Forest District, B.C. from 2002 to 2005 treatment MSMA MSMA MSMA MSMA MSMA MSMA reference reference reference reference a
age/spp
geometric mean n morbidity total [As] range total [As]
adult MPB 15 adult MPB 6 larval/pupal 5 MPB larval/pupal 32 MPB Ips 4 other insects 5 adult MPB 6 adult MPB 4 larval/pupal 11 MPB Cleridae 2
dead live dead
155.50 43.22 93.14
57.3-354.1 7.09-140.3 9.1-700.2
live
20.00
1.3-327.4
live live dead live live
5.92 10.15 0.11 0.75 0.15
0.63-19.6 0.22-62.9 NDa-1.06 0.32-1.06 0.04-0.79
0.36
0.08-1.62
live
ND ) nondetectable.
represent the pentavalent and trivalent forms jointly. Quality control consisted of analysis of a certified reference material (Oyster tissue NIST 1566a) and the in-house standard (Kelp powder), both of which have been previously quantified for organic arsenic species (23). Data Analysis. All of the total arsenic concentrations in bark beetles and blood samples were log-normally distributed and subsequently transformed prior to performing statistical analyses. The data are reported as back-transformed geometric means and ranges where appropriate. Comparisons among beetle samples for effect of treatment, timing of collection, life stages, and species were initially analyzed using a series of one-way analyses of variances (ANOVA) or twosample t-tests. The significance level (0.05) was Bonferroni corrected (0.01) to adjust for multiple comparisons on the data set. We used a two-way ANOVA to examine the effects of treatment with MPB life stage (adult or larval/pupal) and treatment with species (MPB or other insects). We then used a multifactor regression model to test for combined effects of treatment (MSMA or reference), year, morbidity of beetles, and species (MPB or other insects) to identify which variables were most important in predicting total arsenic concentrations. A Pearson correlation analysis identified the relationship between debarking scores of MSMA treated trees approximately 1 year after treatment and the associated concentration of arsenic in MPBs from those trees, excluding all non-MPB and one extreme outlier (700 ppm with debarking score of 5). Blood arsenic residues from male and female breeding pairs (n ) 12 pairs) across all species were significantly positively correlated (r ) 0.64, p ) 0.02). Therefore, in cases where data was available for both the male and female from the same nest, we used an average of the blood arsenic residues and treated the pair as a single sample for statistical analyses. Comparisons among bird species and sexes for total arsenic concentrations in blood were analyzed using a twoway ANOVA. Bird nest locations and recent MSMA treatments (2002-2004) were mapped using ArcMap, and the number of MSMA trees within 1 km2 (564-m radius) of the nest site was summed to examine correlations with blood arsenic residues.
Results Arsenic Residues in Bark Beetles. In total, 90 composite bark beetle samples were collected over 4 years and were analyzed for total arsenic (Table 1). Concentrations of total arsenic in adult and larval MPB from MSMA treated trees ranged from 1.3 to 700.2 µg g-1 dw (geometric mean 42.0 µg g-1) (Table 1). Over half (54%) of the bark beetle samples 1496
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FIGURE 1. Geometric mean concentrations of total arsenic in all samples of adult and larval/pupal stages of Mountain Pine Beetle from MSMA and reference trees collected in the Cascades Forest District, B.C., 2002-2005. Numbers above bars refer to sample sizes within each group. from MSMA trees had arsenic residues 1200 µg g-1 in phloem) (19). The high concentrations and large degree of variability in our MPB samples, collected both alive and dead, suggests that variation in application rates, timing of treatments, procedures, or translocation of MSMA may be occurring in our study area, which could be contributing to the variation in arsenic concentrations and beetle survival. In addition, some beetles may be resistant to MSMA treatment and require much higher doses to cause mortality. Most studies examining the impact of MSMA to bark beetles only measure total arsenic and not specific forms that may be toxicologically more relevant. As previously mentioned, arsenic is present in several chemical forms in the natural environment and its toxicity is dependent on both the arsenic species and the oxidation state (5, 8). It is analytically difficult to determine the oxidation state, which restricts our ability to interpret the absolute toxicity of the arsenic forms we identified in this study. However, consistent with Manville et al.’s (20) identification of the arsenic species in phloem of MSMA and control trees, we found distributions of arsenic species in our beetles that were very similar. Arsenicals are readily transformed through as series of oxidation, reduction, methylation, and demethylation reactions where intermediate metabolites can inherently cause direct toxicity to the organism (8, 9). Therefore, the mortality of bark beetles in MSMA trees is likely, in part, a product of these biotransformation reactions. Since MSMA bioaccumulates in the bark beetles and is not extensively metabolized, bark beetle predators will be readily exposed to high concentrations of monomethyl arsonic acid (MMAA) where it may undergo future transformations. Forest Bird Exposure. Since many of the MPB larvae were able to survive MSMA treatment and accumulate very high concentrations, insectivorous predators are potentially at risk for toxic effects if consuming contaminated beetles regularly and in large quantities. Several species including Hairy, ThreeToed, and Black-Backed (Picoides arcticus) woodpeckers are known to prey upon larval, pupal, and adult stages of bark and wood-boring beetles with diets often consisting of >75% beetle larvae by volume (16). Therefore, woodpeckers could potentially ingest many thousands of beetle larvae during a single day of foraging (26). It appears that woodpecker predation, as evidenced by the degree of debarking, was reduced on trees containing beetle samples with higher concentrations of arsenic. This suggests that although woodpeckers were foraging on MSMA trees, they likely were not consuming the most contaminated 1498
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beetles on a regular basis. Some of the treated trees were heavily debarked (up to 80%), but it is not known whether one or many woodpeckers feed on a single tree and we do not know the frequency of feeding. Reports of woodpeckers aggregating in beetle-infested areas and local densities increasing up to 30 fold (26, 27) suggest that heavy debarking of single trees is probably done by more than one individual. In general, there is limited published data for comparison of arsenic residues in blood of birds. Given the available evidence, we determined that blood arsenic concentrations in most woodpeckers and other forest passerines breeding near MSMA sites were moderately elevated. Seventy-nine percent (42/53) of the individual blood samples were above 0.07 µg g-1 dw, which has been identified as the mean reference value for blood arsenic in control birds from a 2-week MMAA oral dosing study of adult Zebra finches (Taeniopygia guttata) (28). Fifty-one percent (27/53) were greater then 0.14 µg g-1, 2 times higher than this reference value. The forest bird blood levels were within the range found in the Zebra finch’s low and medium dose groups consuming 8 and 24 µg MMAA g-1 bw day-1 (28). Most blood samples were also above other reported reference concentrations; for example, Franklin’s gulls (Larus pipixcan) sampled at an uncontaminated marsh site in the United States had 0.005-0.02 µg g-1 dw (29). Total arsenic concentrations in blood of 11 species of birds sampled near a toxic spill from a mine site exhibited a range of concentrations, 0.006-0.19 µg g-1 dw, that were also generally less than most of our samples (30). Among 109 King (Somateria spectablilis) and Spectacled (Somateria fischeri) eider blood samples collected from a marine system in northern Alaska, only two birds had detectable concentrations of arsenic in blood at 0.55 and 0.80 µg g-1 dw (assuming 80% moisture) (31). Since arsenic is a naturally occurring element with wide geographical differences in background concentrations, it would have been preferable to sample woodpeckers and other passerines in forests without MSMA application to obtain a representative reference value. Nevertheless, given we are studying terrestrial birds, particularly passerines with direct oral exposure to the metabolite MMAA, we believe the concentration of arsenic (0.07 µg g-1) in control birds from the Zebra finch laboratory study is probably the best comparative reference value available at this time. We expected that woodpecker species that consume bark beetles in large quantities (i.e., Three-Toed and Hairy woodpeckers) would have blood arsenic residues positively correlated to MSMA tree density. However, we found large variability in the levels of arsenic from birds sampled in our study area, and blood arsenic residues did not associate positively with species or MSMA tree density, despite data showing that Three-Toed and Hairy woodpeckers feed heavily on MPB and other bark beetles during outbreaks (16, 17, 32-34). This is in contrast to Red-Naped sapsuckers which tend to feed more on sap and other insects, berries, and spiders or chickadees and nuthatches which also have a more varied diet of insects, seeds, nuts, berries, and spiders (16). The highest blood arsenic residue was detected in a female Red-Naped sapsucker, which raises the question of whether another exposure route (i.e., ingestion of sap) is potentially equally or more important than the hypothesized main route of exposure from bark beetle consumption. Variation in toxico-kinetics of organic arsenicals, specifically rates of uptake and elimination, likely contributed to the variance among individual bird blood samples. Ingested methylated arsenicals typically have biological half-lives of only 30 h (35). MSMA is water soluble and readily absorbed by the gastrointestinal tract of mammals with rapid uptake and elimination curves identified for sheep, goats, and rabbits (36, 37). Similarly for birds, adult Zebra finches orally dosed with MMAA at 8, 24, and 72 µg g-1 rapidly accumulated arsenic
in the blood and tissues in a dose-dependent manner (28). However, on the basis of a mass balance approach, finches also rapidly excreted over 90% of the arsenic detected. Rapid accumulation of inorganic arsenic has also been reported in Mallard ducks (Anas platyrhynchos) from dietary exposure of 300 µg g-1 sodium arsenate (38). Mean arsenic concentrations in blood were 0.85 µg g-1 dw and equilibrium levels were typically around 1 µg g-1, but arsenic was also lost rapidly following cessation of exposure (half-life of 1-3 days) (38). The exposure of insectivorous birds foraging in MSMA treated stands will tend to be intermittent rather than continuous. Given the apparent rapid elimination of the chemical, we can infer that any findings of arsenic in blood significantly above reported background levels are strong evidence of recent feeding in MSMA treated stands. However, because of the rapid elimination of the chemical, blood arsenic levels of wild birds only indicate recent exposure and are not appropriate for inferring quantitatively the amount of MSMA they are ingesting. In summary, we detected high arsenic accumulations in bark beetles (both adult and larvae) from MSMA trees, bark beetles surviving relatively high levels of arsenic, evidence of woodpecker foraging on MSMA trees through bark scaling, and elevated arsenic concentrations in blood samples from insectivorous birds breeding near MSMA treatment areas. Our data on blood arsenic values were in the range of arsenic concentrations reported for adult Zebra finches dosed with 8 and 24 µg MMAA g-1 day-1, where significant mass loss occurred at 24 µg g-1 day-1 (28). On the basis of the same study, nestling growth is also expected to be affected by MSMA at 8 µg g-1day-1, relevant to what developing woodpeckers in our study area are predicted to be receiving (4). Taken together, these data suggest that under current environmental conditions exposure of woodpeckers and other insect gleaning species to organic arsenic is likely occurring and may have toxicological consequences.
Acknowledgments We thank the Pesticide Science Fund, Canadian Wildlife Service (Environment Canada), and Science Horizons internship program who provided funding for the project. S. Lee, A. Newbury, M. Wong, T. Sutherland, S. Carroll, and J. Berge assisted in the field research. S. White, J. Komaromi, and D. Shervill contributed to the GIS component. The Ministry of Forests and Range (Merritt office) and several timber operators including BCTS, Tolko, and Weyerhauser provided logistical advice and assistance including data and maps showing locations of MSMA treatment and areas of new MPB infestations.
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Received for review August 15, 2006. Revised manuscript received October 24, 2006. Accepted November 2, 2006. ES061967R
