DDT Toxicity to Perching Birds and Soil Preliminary Remedial Goals (Prgs), Velsicol Site, St

UNITED STATES ENVIRONMENTAL PROTECTION AGENCY REGION 5

DATE: March 25, 2011

SUBJECT: DDT Toxicity to Perching Birds and Soil Preliminary Remedial Goals (PRGs), Velsicol Site, St. Louis, Michigan.

FROM: James Chapman, Ph.D., Ecologist

TO: Tom Alcamo, RPM

Conclusions

A spatially-averaged 5 mg/kg total DDT soil concentration is recommended for a preliminary remedial goal (PRG) for acceptable robin reproduction and development of offspring.

An initial PRG range of 2-9 mg/kg total DDT in soil for robin reproduction is based on a high quality laboratory toxicological study (performed with Japanese quail showing decreased post- hatch chick survival) and a robin exposure model based on site-specific data on soil-earthworm bioaccumulation. Various field studies of robin exposed to DDT indicate that robin reproduction is not impaired within this range of soil DDT concentrations or, in some cases, even somewhat higher. However, an important uncertainty, not adequately addressed by field or laboratory studies, is whether the exposure levels that do not adversely affect robin reproduction are adequately protective for long-term survival and the reproductive performance of offspring. Some studies indicate, but, as yet do not prove, that developmental effects may occur in offspring at some exposure levels that do not impair parental reproduction, which might result in neurobehavioral impairment. The studies indicate that the possible onset of developmental effects might begin within the upper portion of the initial PRG range given above, but there is too much uncertainty to develop specific PRG values.

A laboratory study of ring doves performed with a single exposure treatment at a dose intermediate to the ones bracketing adverse effects in the Japanese quail study also showed decreased post-hatch chick survival. The soil PRG for Velsicol conditions derived from this study is 5.6 mg/kg. Selection of this PRG decreases the likelihood of encountering the possible developmental effects indicated by the aforementioned studies.

Background

This memo presents additional refinement of soil preliminary remedial goals (PRGs) for DDT based on risk to songbirds as a follow-up to Michigan Department of Environmental Quality (MDEQ) (undated) Revised Approach for Calculating DDT Soil Preliminary Remedial Goals (hereafter referred to as “MDEQ Revised Approach”), which was prepared in response to U.S. EPA (12/10/08) Approach for Calculating DDT Soil Preliminary Remedial Goals. Additional laboratory and field studies have been reviewed and a summary is presented of relevant studies.

DDT TRVs and PRGs for passerines edited edited.doc 2

Songbirds are conspicuously absent from the lists of sensitive species to DDT-related reproductive impairment. In contrast to raptors or fish-eating birds, DDT-induced egg-shell thinning is not the mechanism of reproductive toxicity in American robins (Turdus migratorius, thrush family: Turdidae), instead, reproductive impairment may result from embryonic mortality (low hatch rates), nestling mortality (low fledge rates), adult mortality that interrupts nesting and brood care, or developmental effects that impair neurobehavioral processes. These effects occur at higher levels of exposure to DDT compared to the exposures causing eggshell thinning in sensitive species. For example, brown pelicans (Pelecanus occidentalis) may suffer reproductive failure with egg DDE residues less than 4 µg/g (Blus 1996). In contrast, robin clutch size, nest success, hatching rate, and fledge rate were not adversely affected by egg residues an order of magnitude higher: geometric mean total DDT residues of 45 µg/g fresh weight (fw) (87 % DDE) (Gill, et al. 2003).

Field studies of robin reproduction indicate robins are less sensitive to DDT compared to the species susceptible to eggshell thinning. However, an important uncertainty not adequately addressed by field studies is whether the levels of exposures to DDT that appear to be acceptable for reproduction are adequately protective over the full life cycle. In addition to acceptable reproduction, the long-term survival of the offspring and their reproductive performance determine the sustainability of local populations.

To date, field studies have not shown significant impacts of DDT exposures in robins on immune system functions, so this potentially important endpoint is not discussed further in this memo.

Laboratory Studies

The ideal source of toxicity data would be laboratory studies of chronic DDT exposures to American robins, but none were located. The second choice would be studies of related species in the thrush family (Turdidae) (none located), and, third, species from the same taxonomic order as robins –perching birds (Passeriformes). Only a very small number of laboratory DDT studies have been preformed with passerines. The most promising, a study of white-throated sparrows (Mahoney 1975), did not prove to be suitable as discussed below. Therefore, studies of birds in other taxonomic orders in which egg shelling thinning is not responsible for DDT reproductive impairment were reviewed, including studies of chicken, quail (both Galliformes), pigeon, and dove (both Columbiformes).1

Japanese Quail (Cortunix cortunix japonica)

The highest quality study reviewed for this memo, Ueda, et al. (2005), followed a draft revision of the Japanese quail one-generation reproduction test guideline by the Organization for Economic Co-operation and Development (OECD 2000).2 The study is high quality because of

1 The taxonomy of birds is under revision as new data and improved methods are applied to discern evolutionary relationships among birds. The taxonomic orders used in this memo are an older classification (Blair, et al. 1968), however, the newer approaches also show that pigeons, doves, quail, or chicken are not closely related to thrushes (Cracraft and Donoghue 2004). 2 Ueda, et al. (2005) was published too late for inclusion in the literature review for the DDT Eco-SSL (U.S. EPA 2007a). 3

the detailed protocols regarding husbandry and study design, quality control measures such as verification of nominal dietary exposure concentrations and study acceptance criteria based on the performance of the control group, and comprehensive data presentation including bodyweight-normalized doses for each treatment. Three experiments were performed: acute toxicity, subchronic toxicity, and one-generation reproduction studies, all with dietary exposure to p,p’-DDT. The range of doses included in the reproduction study was informed by the results of the first two experiments. The 5-day dietary p,p-‘DDT median lethal concentration (LC50) 3 was 520 ppm dry weight (dw), and the concentration lethal to 10 % of exposed birds (LC10) was 205 ppm dw. Based on the bodyweight-normalized doses reported for the subchronic toxicity study, the LC10 corresponds to 26 – 31 mg/kgBW-d for male and female quail, respectively (BW – bodyweight; d – day). The lowest observed adverse effect level (LOAEL) of the reproduction study was 30 ppm dw diet, based on a statistically discernible doubling of chick mortality through 14 days after hatching (40-41 % chick mortality with 4-5 weeks parental DDT exposure compared to 18-21 % control chick mortality over the same time periods). The no observed adverse effect level (NOAEL) was 6 ppm dw diet. The bodyweight normalized toxicity reference values (TRVs) for reproduction are 0.84 – 4.5 mg/kgBW-d, NOAEL – LOAEL, respectively (Ueda, et al. 2005). Incorporation of the TRVs into the Velsicol site-specific DDT bioaccumulation model for robin results in a soil PRG range of 2 – 9 mg/kg (rounded values).

White-throated Sparrow (Zonotrichia albicollis)

The MDEQ Revised Approach relied on TRVs based on adverse growth effects in white- throated sparrows exposed to technical DDT 4 (Mahoney 1975), adopted from the calculations presented in the Ecological Soil Screening Level (Eco-SSL) for DDT (U.S. EPA 2007a). Reduced growth was reported with 5 ppm dw technical DDT in feed. However, on review of this study, the growth effects are not biologically relevant and are unsuitable for baseline risk assessment purposes. There are two issues. Statistically significant differences were reported for a single sample period, after 5 weeks of exposure to DDT, but differences in growth were not statistically discernible in any of the subsequent 5 sampling periods through 11 weeks exposure, or in any of the 5 sampling periods earlier than 5 weeks (Mahoney 1975). A single statistically significant difference out of 11 sample times might be acceptable for screening purposes,5 but is dubious for baseline risk assessment. The second issue concerns the magnitude of the growth effects. Mahoney (1975) reported transformed data (arcsine √(% weight change + 0.2)), but not the original untransformed growth data. Back transformation 6 of the data in Mahoney (1975)

3 Ueda, et al (2005) did not report the moisture content basis for dietary DDT concentrations as recommended by OECD (2000), but the reported treatment feed intake rates are consistent with dry-weight food ingestion values, and the reported bodyweight-normalized chemical intake rates can be verified from the respective treatment feed intake and dietary DDT data if the dietary DDT units represent dry-weight concentrations. 4 78 % p,p’-DDT and 21 % o,p’-DDT or p,p’-DDE (Mahoney 1975). 5 Although included in the literature review, Mahoney (1975) was not used to derive the DDT Eco-SSL (U.S. EPA 2007). 2 6 % weight change = (sin Y) - 0.2, where Y is a transformed value in Mahoney (1975) Figure 1. 4

Figure 1 shows less than 0.2 % difference in growth between treatment and control after 5 weeks exposure, which is not biologically meaningful regardless of the level of statistical significance.7

DDT feeding studies with two European passerine birds, European robin (Erithacur rubecula) and common redstart (Phoenicurus phoenicurus) (both thrush family: Turdidae) provide supporting information that growth effects are unlikely at the dose reported by Mahoney (1975). Adult European robins gained weight with 15 days exposure to 0.7 mg pp’-DDT/kgBW-d (Södergren and Ulfstrand 1972),8 and an equivalent dose reportedly had no effect on bodyweight of adult common redstarts after 12 days exposure (Karlsson, et al. 1974).9 Only a single exposure treatment was included in each study, so the doses resulting in bodyweight loss are unknown (some value >0.7 mg/kgBW-d). The unbounded NOAEL of these studies approaches the 1 mg/kgBW-d purported LOAEL of the Mahoney (1975) study calculated by Eco-SSL (U.S. EPA 2007a), and is substantially greater than the 0.2 mg/kgBW-d extrapolated NOAEL in the MDEQ Revised Approach.

Mahoney (1975) also reported an increase in nocturnal activity in DDE-exposed sparrows, but the ecological impacts of this behavioral effect are unknown.

Mahoney (1975) reported a dramatic decrease in fat accumulation – after 5 weeks, sparrows exposed to 25 ppm dw technical DDT in feed had only about one-half of the fat levels of control sparrows, while fat accumulation was unimpaired at 5 ppm DDT. Mahoney (1975) reportedly measured food consumption, but did not publish the data, so the bodyweight-normalized doses have to be estimated. Incorporating the dose conversion for this study reported by Eco-SSL (U.S. EPA 2007a) and the site-specific bioaccumulation model for Velsicol, the TRVs correspond to soil PRGs of 2 – 11 mg/kg. However, a companion paper showed equivalent levels of fat accumulation in all treatments after 11 weeks exposure (Mahoney 1974) complicating interpretation of the potential significance.

In discussions with MDEQ, alternative sources of DDT TRVs were proposed including Jefferies and French 1971 (pigeon), Davison, et al. 1976 (Japanese quail), and Cecil, et al. 1978 (chicken), as presented in the literature review of the Eco-SSL for DDT (U.S. EPA 2007a). Each study has been reviewed for this memo.

Homing Pigeon (Columbia livia)

Jefferies and French (1971) reported increased mortality of pigeons at the highest dose of 36 mg p,p’-DDT/kgBW-d and no mortality at 18 mg/kgBW-d. These data are mistakenly normalized to bodyweight a second time in the Eco-SSL literature review (U.S. EPA 2007a), giving

7 The observed growth differential would be biologically meaningful if Mahoney (1975) misreported the units of the weight change data as “%” when it was decimal fraction weight change instead. However, recommendations for remedial action can not be based on an assumed editorial error. 8 10.5 µg pp’-DDT/d ÷ 15.0 g initial mean bodyweight (Söndergren and Ulfstrand 1972). 9 10.5 µg pp’-DDT/d (Karlsson et al. 1974) ÷ 15.5 g weighted mean bodyweight for males and females (calculated from Garamszegi, et al. 2005 Table 2). Karlsson, et al. (1974) measured bodyweight daily and stated there were no differences among treatments, but did not show the data 5

erroneously low TRVs for mortality.10 The original adult mortality TRVs correspond to a soil PRG range of 37 – 74 mg/kg for Velsicol conditions.

Japanese Quail

Davison, et al. (1976) reported increased egg breakage by Japanese quail caged in pairs at 40 ppm p,p’-DDT dietary exposure, but not at 10 ppm. The increased breakage was not due to eggshell thinning, but apparently a result of behavioral effects. Food ingestion rates were not reported, so the bodyweight-normalized doses have to be estimated. Using the dose estimates for this study calculated in Eco-SSL (U.S. EPA 2007a) and the Velsicol site-specific bioaccumulation model, the soil PRG range is 3 – 11 mg/kg. In addition to uncertainty over bodyweight-normalized dose, DDT-associated egg breakage was not observed in caged pairs of a second strain of Japanese quail or in individually-caged quail of either strain (Davidson, et al. 1976). The consistency of this effect and applicability to other species are not clear. Japanese quail egg breakage was not statistically elevated in Ueda, et al. (2005), even at higher doses than those tested by Davison, et al. (1976). Besides possible strain differences, the 263-428 cm2 floor area per bird for Davison, et al. (1976) caged pairs is much smaller than the OECD (2000) recommended 625 cm2/bird for caged pairs of Japanese quail above 4 weeks age. OECD (2000) cautions that pen mate aggression can be a problem in Japanese quail experiments. The egg breakage reported by Davison, et al. (1976) is an inconsistent effect that may have been related to suboptimal rearing conditions for Japanese quail.

TRVs for survival based on Davison, et al. (1976) are also reported in EcoSSL (U.S. EPA 2007a), however, across 4 experimental designs (2 strains of quail caged individually and in pairs), control mortality ranged from 0 to 8 %, and DDT-exposed mortality ranged from 0 to 8 % (calculated from their Tables II and III). The low levels of mortality appear to be random and unrelated to the DDT doses included in this study. In their reproduction study, Ueda, et al. (2005) reported only 1 death of 36 mature birds (3 % mortality) at 150 ppm dw, an exposure concentration almost 4 times greater than the 40 ppm dw maximum in Davison, et al. (1976), which is a further indication that the Davison, et al. (1976) mortality was probably not related to DDT exposure.

Chicken (Gallus domesticus)

Cecil, et al. (1978) reported statistically greater bodyweight loss in mature chicken at 50 ppm p,p’-DDT in diet compared to controls after 30 days exposure. 11 All treatments including controls lost weight during the experiment, but the mean final bodyweight of the 50-ppm treatment was 7 % less than control bodyweight. Weight loss at 5 ppm diet was not statistically discernible from control weight loss. Food ingestion rates were not measured, so the bodyweight-normalized doses have to be estimated. Using the dose estimates for this study calculated in Eco-SSL, 0.23 – 2.3 mg/kgBW-d (U.S. EPA 2007a), and the Velsicol site-specific bioaccumulation model, the soil PRG range is 0.5 – 5 mg/kg. The study has several limitations –

10 Although included in the literature review, Jefferies and French (1971) was not used to derive the DDT Eco-SSL (U.S. EPA 2007). 11 The Eco-SSL DDT soil screening value is derived from this study (U.S. EPA 2007). 6

weight loss in control birds indicates the rearing conditions were not optimal, the bodyweight- normalized doses are uncertain, and the sample size is very low, only 5 birds per exposed treatment. It should be noted that the study was not designed to rigorously determine the impacts of DDT exposure on chicken growth, the objective was to investigate induction of liver enzymes by DDT and PCBs.

Cecil, et al. (1978) also reported high mortality of mature chicken at 500 ppm p,p’-DDT in diet, but no mortality at 50 ppm diet. The adult survival TRVs, 2.3 – 23 mg/kgBW-d, correspond to a soil PRG range of 5 – 47 mg/kg for Velsicol conditions.

Ring Dove (Streptopelia risoria)

An additional study, not suggested by MDEQ, is reviewed. Haegele and Hudson (1973) reported multiple effects of 126-day exposure to 40 ppm p,p’-DDE in diet on ring dove reproduction including fewer nestings, few eggs laid, and 44 % decrease in chick survival – mostly within the first 8 days after hatching. The combined effect resulted in 71 % fewer live young 21 days after hatching for DDE-exposed birds compared to unexposed controls. Unfortunately, only one exposure treatment was included in the experiment. Food ingestion rates were not measured, so the bodyweight-normalized dose has to be estimated. A 2.7 mg/kgBW-d bodyweight-normalized dose for 40 ppm dietary exposure was calculated based on the 0.068 kg/kgBW-d food consumption reported for DDE-exposed ring doves (20 and 200 ppm in diet) in another study (Heinz, et al. 1980). A NOAEL is not available because only a single exposure treatment was investigated; however, the study is included in this review because the estimated dose, 2.7 mg/kgBW-d, is intermediate between the NOAEL and LOAEL of Ueda, et al. (2005) and includes the same toxicological endpoint – chick mortality. The Haegele and Hudson (1973) LOAEL TRV corresponds to a 6 mg/kg soil PRG for Velsicol conditions.

Field Studies

Field studies of DDT and American robins have been reported for vector control of Dutch elm disease in residential and institutional settings, spruce budworm control in northern forests, and legacy DDT in fruit orchard soils. No single field study has sufficient information to fully support derivation of soil PRGs, but the studies provide supplemental information for interpreting the risk management implications of laboratory studies of other bird species.

Dutch Elm Disease Control

Bird deaths were an early reported side effect of heavy DDT spraying (Hotchkiss and Pough 1946). DDT applications for Dutch elm disease vector control resulted in high robin mortality and depressed robin populations in spray areas (Baker 1958, Wallace, et al. 1961, Wurster, et al. 1965, Hunt 1969, Beaver 1980). A key pathway for lethal exposure to robins was consumption of earthworms that accumulated DDT through feeding on leaf fall from sprayed trees (Baker 1958), which provides an explanation for the observed delays between initiation of DDT spray programs and increased robin deaths. The lethality of earthworm-accumulated DDT to robins was confirmed by laboratory feeding studies with other birds (Boykins 1967). DDT appeared to have “no detectable effect on clutch size in robins”, instead, the adverse effect of DDT exposure 7

on robin reproduction was “mediated through the death of the parents”, which curtailed incubation of eggs and care of nestlings (Beaver 1980).

DDT concentrations in earthworms steadily declined after DDT spraying was discontinued, and, within 5-6 years, robin survival increased to sustainable levels (Beaver 1980). Effect thresholds can be approximated from data on robin pre-nesting and nesting population sizes and concurrent DDT concentrations in earthworms on the Michigan State University north campus (Beaver 1980 Figure 1). The apparent field LOAEL for robin mortality is 31 ppm ww (wet weight) earthworm DDT concentration (the pre-nesting and nesting adult robin abundance 95 percent confidence limits (95CLs) are non-overlapping showing significant mortality (>50 %) of robins between spring arrival and nesting), and 4.9 ppm ww earthworm DDT concentration is an unambiguous NOAEL (no difference between pre-nesting and nesting adult robin abundances). Applying a 0.77 soil-to-earthworm accumulation factor (dw-to-ww) for Velsicol conditions, the range of earthworm DDT concentrations corresponds to soil dry weight (dw) DDT concentrations of 6 – 40 ppm. Intermediate earthworm DDT concentrations, approximately 15 ppm ww, were accompanied by high mortality (the pre-nesting adult robin populations declined by 30-50 % to the nesting periods), but the population differences apparently were not statistically discernible (the pre-nesting and nesting adult robin abundance 95CLs overlap). In a strict sense, the corresponding soil DDT concentration, 20 ppm dw for Velsicol conditions, represents a statistically-based no effect level for robin mortality, but this may be an artifact of the large daily variability associated with the population census method that limits the statistical power of the field observations. The possibility that 20 ppm DDT soil concentrations may be harmful to adult robins, as indicated by high apparent mortality, cannot be confidently excluded by the data reported by Beaver (1980).

A conservative interpretation of the MSU field data combined with Velsicol site-specific soil- earthworm bioaccumulation is that a soil DDT concentration of 6 mg/kg is unlikely to affect robin reproduction, 20 mg/kg may be near the threshold for adverse effects, and 40 mg/kg is associated with severe population impacts through curtailment of the reproductive cycle by early mortality of parental robins.

Fledgling success or long-term survival of robins from sprayed areas apparently were not investigated.

Spruce Budworm Control

Maine forests were sprayed with DDT for spruce budworm control between 1958 and 1967. Analyses of robin eggs collected from sprayed and unsprayed areas showed no significant relationship between DDT (∑ DDT, DDE, DDD) concentration and eggshell thinning, and no difference in eggshell weight compared to archived robin eggshells collected in Maine prior to 1900 (Knupp, et al. 1976), i.e., before DDT insecticide use. Robin egg hatchability was not affected by DDT as evidenced by a low rate of hatch failure (6 %) in sprayed areas, and a lower mean DDT concentration in unhatched eggs compared to viable eggs (Knupp, et al. 1976). Surface soil DDT residues (∑ DDT, DDE, DDD) in sprayed forest areas were as high as 5.9 ppm (Owen, et al. 1977). Although the robin and soil investigations were funded in part under the same grant, the soil and robin data are not directly matched so the results should be cautiously 8

interpreted. However, the data are consistent with Beaver (1980) in indicating no adverse reproductive effects in robins exposed to soils with 6 mg/kg DDT (for Velsicol conditions).

Fledgling success or long-term survival apparently were not investigated.

Legacy DDT in Orchard Soils

DDT was heavily used in fruit orchards, especially apple for codling moth control. Soil residues have persisted decades since agricultural uses of DDT were discontinued. Orchard wildlife continue to accumulate legacy DDT through food chain exposures, and robins have been shown to have higher DDT levels “than in the predatory kestrel or any other bird, mammal, or invertebrate assessed” (Harris, et al. 2000 and references).

An early study of robins in a New York state apple orchard sprayed with DDT, but shifting to replacement pesticides over the 3-year course of the study, showed relatively minor impacts on robin reproductive success (Johnson, et al. 1976). Orchard robins had slightly reduced mean clutch size (3.0-3.4 vs. 3.4-3.7 eggs/nest), but no adverse effects on hatching success or egg-to- fledgling success, and greater nesting success (62-74 vs. 59-66 % of nests with eggs that produced at least 1 successful fledgling) compared to concurrent records of robins in 9 northeastern states. Total DDT/DDE concentration ranged between 2 and 16 mg/kg dw 12 in the soil of the preferred foraging area close to the nest locations, but orchard robins also foraged in more distant areas with soil DDT concentrations below detection limits (Johnson, et al. 1976). Interpretation of the reproductive data is limited by the unknown allocation of foraging in different areas, estimated conversion of soil ww concentrations to dw, and use of regional values for “control” robin reproductive performance instead of a local reference group. Although the results cannot be used to derive acceptable soil DDT values for robin reproductive performance, they do indicate that robin reproduction is not grossly impaired by preferentially foraging in an area with a range of soil DDT concentrations approximately similar to and even somewhat higher than the 2 – 9 mg/kg PRG range based on the Ueda, et al. (2005) Japanese quail toxicity study. Johnson, et al. (1976) tried to collect data on adult survival, but this portion of the study was unsuccessful.

Studies of eastern bluebirds (Sialia sialis, thrush family: Turdidae) in southern Ontario orchards, show a significant positive relationship between egg organochlorine residues (predominantly p,p’-DDE) and incidence of unhatched eggs 13 (Bishop, et al. 2000), and a significant negative relationship between egg p,p’-DDE concentration and corticosterone secretion in nestlings, which could compromise stress responses and potentially disrupt fat accumulation (Mayne, et al. 2004). Unfortunately, soil data were not reported, the orchard locations were not identified preventing use of other orchard soil data, so the results cannot be linked to soil DDT levels. The studies indicate a potential for adverse sublethal effects from exposures to legacy DDT soil residues, in addition to the lethal effects observed in the elm spraying field studies.

12 Johnson, et al. (1976) reported 2-11 ppm ww DDT/DDE in a heavy clay soil with high organic matter in the favored foraging area, converted to dry weight using a range of soil moisture contents of 30 % at field capacity for a silty clay soil (Brady 1974) and 15 % m.c. at one-half field capacity. Robins also foraged in other areas with soil ww DDT concentrations < 1 ppm. 13 Unhatched eggs include infertile eggs, early embryonic death, and eggs missing from the nest. 9

Robins nesting in orchards in Okanagan Valley, British Columbia, Canada, showed no reproductive impairment compared to non-orchard robins for clutch size, eggshell thickness, brood size, hatch rate or fledge rate 14 (Gill, et al. 2003). The mean earthworm total DDT residues (Σ p,p’ and o,p’ isomers of DDT, DDE, DDD) in Okanagan Valley orchards was 11 mg/kg ww 15 (Harris, et al. 2000), which corresponds to 14 mg/kg dw soil for Velsicol conditions. This is identical to the reported mean surface soil total DDT concentration (14.4 mg/kg dw) for Okanagan Valley orchards (Harris, et al. 2000), indicating similar soil DDT bioavailability at Velsicol and Okanagan Valley orchards. Some limitations are the soil/earthworm data and robin reproduction data are not specifically linked (although two of the researchers participated in both studies), soil sample size is low (n = 4), and long-term survival was not investigated. However, the results are consistent with the orchard field study by Johnson, et al. (1976).

An innovative approach for investigating developmental effects of DDT exposures to orchard robins was reported by Iwaniuk, et al. (2006). Eighteen nestlings were taken from Okanagan Valley orchard nests and reared in captivity with clean diets. Early exposure to DDT (and other contaminants) was measured by analysis of eggs taken from the same nests. Significant negative correlations were observed between egg total DDT residues (Σ p,p’ and o,p’ isomers of DDT, DDE, DDD) and/or p.p’-DDE residues and brain development, specifically, whole brain volume, song nuclei 16 volume, and relative forebrain volume in males, and nucleus intercollicularis (ICo) volume in males and females. There were no significant correlations with any other measured egg contaminant. “[T]hese effects are startling, particularly when the exposure to DDT was limited to embryonic and early post-hatching development and the birds were sacrificed in their second year. This suggests that whatever effects DDT is having on the brain during development, the effects are long-lasting” (Iwaniuk, et al. 2006). Some evidence indicates the developmental effect may be due to DDT-induced endocrine disruption, but direct DDT neurotoxicity or indirect stress-related responses cannot be ruled out (Iwaniuk, et al. 2006). Functional impacts on survival or reproduction were not reported, but behavioral observations “suggested that singing rates did decrease with p,p’-DDE levels” (Iwaniuk, et al. 2006). Diminished singing rates could impair courtship and reproductive success. Impairment of ICo could impair courtship behavior (Iwaniuk, et al. 2006) and may, in part, be responsible for abnormal courtship behavior reported for several species of birds exposed to DDT (Zala and Penn 2004). In captivity and on clean diets, the reproductive success of robins from orchard nests reportedly did not differ from captive non-orchard robins, but unspecified behavioral abnormalities were observed in birds from the more highly contaminated nests (data not shown) (Smith, et al. 2001). Although the observed deficits in brain development cannot be quantitatively linked at present to long-term effects, the findings serve as a caution that parental DDT exposures that do not significantly impact robin reproduction and fledge rate may nonetheless affect the offspring through non-lethal developmental effects.

14 Within orchard robins only, a significant trend was observed between fledge rate and egg DDE (and dieldrin), 2 but the low r (0.11) indicates “minimal biological significance” (Harris, et al. 2003). 15 Mean of multiple species of earthworms, reported as 62.9 mg/kg dw (Harris, et al. 2003), converted to ww assuming 82 % moisture content in earthworms (midpoint of the 75-90 % range in Edwards and Bohlen 1996). 16 Nucleus robustus arcopalliallis (RA) and higher vocal center (HVC) (Iwaniuk, et al. 2006). 10

Iwaniuk, et al. (2006) did not measure the soil DDT concentrations surrounding the nests that provided the nestlings for their study, but a rough calculation can be made using their egg data and empirical bioaccumulation factors (BAF) reported for Okanagan Valley orchards. The range of total DDT residues in robin eggs, 15-175 mg/kg ww (Iwaniuk, et al. 2006), correspond to 0.4- 4.5 mg/kg ww in earthworms based on an overall mean earthworm-egg total DDT BAF of 39.74 dw/dw (Harris, et al. 2000),17 which, in turn, corresponds to 0.5-6.0 mg/kg dw soil for Velsicol conditions (soil-to-earthworm BAF of 0.77 ww/dw).18 However, there is large variability in the earthworm-to-robin egg total DDT BAFs within the Okanagan Valley orchards – location- specific mean BAFs ranged from 14.6 to 85.0 dw/dw (Harris, et al. 2000), and the corresponding soil DDT concentrations range from 1-16 mg/kg to 0.2-3 mg/kg, respectively, for Velsicol conditions. Taking into account variability in earthworm-to-egg BAF, the estimated total DDT soil concentration corresponding to the upper end of the Iwaniuk, et al. (2006) egg contaminant data is 3-16 mg/kg with a central estimate of 6 mg/kg. Since the threshold brain size reduction resulting in significantly reduced long-term survival or reproductive success is unknown (the lack of reproductive effects reported by Smith, et al. (2001) applies to birds that have no further exposure to DDT 10 days after hatching, unlike nestling raised in a contaminated orchard), the extrapolated soil values are probably best interpreted as indicators of the possible onset of neurobehavioral impairment. The soil DDT range overlaps with the levels associated with successful robin reproduction in field studies, as discussed above, which indicates, but does not prove, that some levels of exposure to embryos and early nestling-stages may potentially result in long-term behavior effects in offspring even though the reproductive success of the parents was not adversely affected.

Literature Cited

Barker, R. 1958. Notes on some ecological effects of DDT sprayed on elms. J Wildl Manage 22: 269-274.

Beaver, D. 1980. Recovery of an American robin population after earlier DDT use. J Field Ornithol 51: 220-228. and comment: G. Wallace. 1983. On the status of American robins at Michigan State University. J Field Ornithol 53: 173.

Bishop, C.A., B. T. Collins, P. Mineau, N. M. Burgess, W. F. Read, and C. Risley. 2000. Reproduction of cavity-nesting birds in pesticide-sprayed apple orchards of southern Ontario, Canada. Environ Toxicol Chem 19: 588-599.

Blair, W., A. Blair, P. Brodkorb, F. Cagel, and G. Moore. 1968. Vertebrates of the United States, 2nd ed. McGraw-Hill, New York. 616 p.

17 Robin egg wet-weight DDT concentrations are converted to a dry-weight basis using a mean moisture content of 82.5 % for Okanagan Valley robin eggs (Harris, et al. 2000). 18 The calculated earthworm dry-weight DDT concentrations are converted to a wet-weight basis using a midpoint moisture content of 82 % (75-90 % range in Edwards and Bohlen 1996). 11

Blus, L. 1996. DDT, DDD, and DDE in birds. In: Environmental Contaminants in Wildlife, Interpreting Tissue Concentrations. Beyer. (Eds.: W.N., G. Heinz, and A. Redmon-Norwood). Lewis, Boca Raton. Pp. 49-71.

Boykins, E. 1967. The effects of DDT-contaminated earthworms in the diet of birds. BioSci 17(1): 37-39.

Brady, N. 1974. The Nature and Properties of Soils, 8th ed. MacMillian Publ., New York. 639 p.

Cecil, H., S. Harris, and J. Bitman. 1978. Liver-mixed function oxidases in chickens: Induction by polychlorinated biphenyls and lack of induction by DDT. Arch Environ Contam Toxicol 7: 283-290.

Cracraft, J. and M. Donoghue (eds.). 2004. Assembling the Tree of Life. Oxford Univ. Press, New York. 576 p.

Davison, K., K. Engebretson, and J. Cox. 1976. P,p-DDT and p,p-DDE effects on egg production, eggshell thickness, and reproduction of Japanese quail. Bulletin of Environmental Contamination and Toxicology 15: 265-270.

Edwards, C. and P. Bohlen. 1996. Biology and Ecology of Earthworms, 3rd ed. Chapman & Hall, New York. 426 p.

Garamszegi, L., M. Eens, J. Erritzøe, and A. Møller. 2005. Sexually size dimorphic brains and song complexity in passerine birds. Behav Ecol 16: 335-345.

Gill, H., L. Wilson, K. Cheng, and J. Elliott. 2003. An assessment of DDT and other chlorinated compounds and the reproductive success of American robins (Turdus migratorius) breeding in fruit orchards. Ecotoxicol 12:113-123.

Haegele, M. and R. Hudson. 1973. DDE effects on reproduction of ring doves. Environ Pollut 4: 53-57.

Harris, M., L. Wilson, J. Elliott, C. Bishop, A. Tomlin, and K. Henning. 2000. Transfer of DDT and metabolites from fruit orchard soils to American robins (Turdus migratorius) twenty years after agricultural use of DDT in Canada. Arch Environ Contam Toxicol 39:205-220.

Heinz, G., E. Hill and J. Contrera. 1980. Dopamine and norepinephrine depletion in ring doves fed DDE, dieldrin, and Arochlor 1254. Toxicol Appl Pharmacol 53: 75-82.

Hotchkiss, N. and R. Pough. 1946. Effect on forest birds of DDT used for gypsy moth control in Pennsylvania. J Wildl Manage 10: 202-207.

Hunt, L. 1969. Physiological susceptibility of robins to DDT poisoning. Wilson Bull 81: 407- 418.

Iwaniuk, A., D. Koperski, K. Cheng, J. Elliott, L. Smith, L. Wilson, and D. Wylie. 2006. The effects of environmental exposure to DDT on the brain of a songbird: Changes in structures associated with mating and song. Behav Brain Res 173: 1-10.

Jefferies, D. and M. French. 1971. Hyper- and hypothyroidism in pigeons fed DDT: an explanation for the ‘thin eggshell phenomenon’. Environ Pollut 1: 235-242.

Johnson, E., G. Mark, and D. Thompson. 1976. The effects of orchard pesticide applications on breeding robins. Wilson Bulletin 88: 16-35.

Karlsson, B., B. Persson, A, Södergren, and S. Ulfstrand. 1974. Locomotory and dehydrogenase activities of redstarts Phoenicurus phoenicurus L. (aves) given PCB and DDT. Environ Pollut 7:53-63.

Knupp, D., R. Owen, Jr., and J. Dimond. 1976. Pesticide dynamics in robins nesting in contaminated and uncontaminated forests in northern Maine. Can J Zool 54: 1669-1673.

Mahoney, Jr., J. 1974. Residue accumulation in white-throated sparrows fed DDT for 5 and 11 weeks. Bull Environ Contam Toxicol 12: 677-681.

Mahoney, Jr., J. 1975. DDT and DDE effects on migratory condition in white-throated sparrows. J Wildl Managem 39: 520-527.

Mayne, G., P. Martin, C. Bishop, and H. Boermans. 2004. Stress and immune responses of nestling tree swallows (Tachycineta bicolor) and eastern bluebirds (Sialia sialis) exposed to nonpersistent pesticides and p,p’-dichlorodiphenyldichloroethylene in apple orchards of southern Ontario, Canada. Environ Toxicol Chem 23: 2930-2940.

OECD. 2000. OECD Guideline for Testing of Chemicals, Proposal for a New Test Guideline, Avian Reproductive Toxicity Test in the Japanese Quail or Northern Bobwhite. Revised Draft Document, April 2000. Organization for Economic Co-operation and Development. www.oecd.org/dataoecd/40/31/2739811.pdf

Owen, Jr., R., J. Dimond and A. Getchell. 1977. DDT: persistence in northern spodosols. J Environ Qual 6: 359-360.

Smith, L., J. Elliot, L. Wilson, K. Cheng. 2001. Effects of DDT exposure on American robins from orchards of the Okanagan Valley, British Columbia. Poster. 22nd Annual Meeting, Society of Environmental Toxicology and Chemistry. 2001. http://abstracts.co.allenpress.com/pweb/setac2001/document/35220

Södergren A. and S. Ulfstrand. 1972. DDT and PCB relocate when caged robins use fat reserves. Ambio 1: 36-40.

Ueda, H., K. Ebino, H. Fujie, K. Hayashi, M. Satoh, N. Nakashima, Y. Chiba, T. Harada, M. Saka, Y. Koma, T. Nagata, Y. Odanaka, and S. Termoto. 2005. Reassessment of ecotoxicities of 13

1,1,1-trichloro-2,2-bis(4-chlorophenyl)ethane in Japanese quail under the OECD draft new avian one-generation reproduction test guideline. Regul Toxicol Pharmacol 41: 167-174.

U.S. EPA. 1993. Wildlife Exposure Factors Handbook. vol. I and II. Office of Research and Development. EPA/600/R-93/187a and b. http://cfpub.epa.gov/ncea/cfm/wefh.cfm?ActType=default

U.S. EPA. 2007a. Ecological Soil Screening Levels for DDT and Metabolites. U.S. Environmental Protection Agency, Office of Solid Waste and Emergency Response. OSWER Directive 9285.7-57. www.epa.gov/ecotox/ecossl/

U.S. EPA. 2007b. Guidance for Developing Ecological Soil Screening Levels (Eco-SSLs), Attachment 4-1, Exposure Factors and Bioaccumulation Models for Derivation of Wildlife Eco- SSLs. U.S. Environmental Protection Agency, Office of Solid Waste and Emergency Response. OSWER Directive 9285.7-55. www.epa.gov/ecotox/ecossl/pdf/ecossl_attachment_4-1.pdf

Wallace, G., W. Nickell, and R. Bernard. 1961. Bird Mortality in the Dutch Elm Disease Program in Michigan. Bulletin 41. Cranbrook Institute of Science, Bloomfield Hills, MI. 44 p. http://www1.umn.edu/ships/pesticides/library/wallace1961.pdf

Wurster, D., C. Wurster, Jr. and N. Strickland. 1965. Bird mortality following DDT spray for Dutch elm disease. Ecology 46: 488-499.

Zala, S. and D. Penn. 2004. Abnormal behaviours induced by chemical pollution: a review of the evidence and new challenges. Anim Behav 68: 649-664.

Appendices

Soil Preliminary Remedial Goal Calculations for Selected Laboratory DDT or DDE Toxicity Studies Based on Velsicol-specific Robin Exposure Model

Appendix Acronyms and Abbreviations

BAF – biomagnification factor BW - bodyweight CDM – Camp Dresser & McKee Conc - concentration d – day DDE – 1,1-dichloro-2,2-bis(p-chlorophenyl)ethylene DDT – 1,1,1-trichloro-2,2-bis(p-chlorophenyl)ethane DF – dietary fraction dw – dry weight Eco-SSL – ecological soil screening level kg - kilogram LOAEL – lowest observed adverse effect level mc – moisture content mg – milligram na – not available NIR – bodyweight normalized ingestion rate NOAEL – no observed adverse effect level o,p’ – ortho, para p,p’- para, para ppm – parts per million PRG – preliminary remedial goal SFF – site foraging factor TRV – toxicity reference value U.S. EPA – United States Environmental Protection Agency veg – vegetation wk - week worm - earthworm ww – wet weight

CDM Method (Cecil et al. 1978, LOAEL, growth)

NIR (Food) kg ww/kgBW-d 1.205 U.S. EPA 1993

NIR (Food) kg dw/kgBW-d 0.214 Eco-SSL, high-end for woodcock (U.S. EPA 2007b) Site Soil Conc mg/kg dw 9.785 Site

Dietary TRV mg/kgBW-d 2.27 Cecil et al 1978, chicken, adult bodyweight, 50 ppm p,p'-DDT feed Conc Worm mg/kg ww 7.534 =BAF*Soil Conc Conc Plant mg/kg ww 0.289 =BAF*Soil Conc DF Veg mg/kg ww 0.5 Estimated mean DF Worm mg/kg ww 0.5 Estimated mean DF Soil mg/kg dw 0.020 Estimated Soil-Worm BAF ratio ww/dw 0.77 ww, site Soil -to-Plant BAF ratio ww/dw 0.0295 ww, site

Dose mg/kgBW-d 6.807 =(NIRww*Conc Worm*DFworm)+(NIRww*Conc Plant*Dfplant)+(NIRdw*Conc Soil*DFsoil) Soil PRG mg/kg dw 4.7 =TRV/(NIRww*BAFworm*DFworm)+(NIRww*BAFveg*DFveg)+(NIRdw*DFsoil)

CDM Method (Cecil et al. 1978, NOAEL, growth)

Dietary TRV mg/kgBW-d 0.227 Cecil et al 1978, 5 ppm feed Soil PRG mg/kg dw 0.5 =TRV/(NIRww*BAFworm*DFworm)+(NIRww*BAFveg*DFveg)+(NIRdw*DFsoil)

PRG = LOAEL or NOAEL / SUM ((NIRww * BAFPrey1 * DFPrey1…x * SFF) + (NIRdw * DFsoil * SFF)) SFF - site foraging factor = 1.0

Effect - 10 % decrease in weight after 30-d exposure compared to 2 % decrease by controls. The final mean bodyweight at 50 ppm was 7 % less than the final control bodyweight. Uncertainty - food ingestion rate not measured; moisture content not given for DDT concentration

DDT TRVs and PRGs for passerines edited edited.doc 17

CDM Method (Haegele and Hudson 1973, LOAEL, chick survival)

NIR (Food) kg ww/kgBW-d 1.205 U.S. EPA 1993

NIR (Food) kg dw/kgBW-d 0.214 Eco-SSL, high-end for woodcock (U.S. EPA 2007b) Site Soil Conc mg/kg dw 9.785 Site

Dietary TRV mg/kgBW-d 2.7 Haegele and Hudson 1973, ring dove, 40 ppm p,p'-DDE feed, chick survival Conc Worm mg/kg ww 7.534 =BAF*Soil Conc Conc Plant mg/kg ww 0.289 =BAF*Soil Conc DF Veg mg/kg ww 0.5 Estimated mean DF Worm mg/kg ww 0.5 Estimated mean DF Soil mg/kg dw 0.020 Estimated Soil-Worm BAF ratio ww/dw 0.77 ww, site Soil -to-Plant BAF ratio ww/dw 0.0295 ww, site

Dose mg/kgBW-d 6.807 =(NIRww*Conc Worm*DFworm)+(NIRww*Conc Plant*Dfplant)+(NIRdw*Conc Soil*DFsoil) Soil PRG mg/kg dw 5.6 =TRV/(NIRww*BAFworm*DFworm)+(NIRww*BAFveg*DFveg)+(NIRdw*DFsoil)

CDM Method (Haegele and Hudson 1973, NOAEL, chick survival)

Dietary TRV mg/kgBW-d na Soil PRG mg/kg dw

PRG = LOAEL or NOAEL / SUM ((NIRww * BAFPrey1 * DFPrey1…x * SFF) + (NIRdw * DFsoil * SFF)) SFF - site foraging factor = 1.0

Effect - 44 % decrease in chick survival Uncertainty - food consumption not reported, dietary mc not reported, only one exposure treatment, dose extrapolated from Heinz, et al. 1980

CDM Method (Ueda et al. 2005, LOAEL, reproduction)

NIR (Food) kg ww/kgBW-d 1.205 U.S. EPA 1993

NIR (Food) kg dw/kgBW-d 0.214 Eco-SSL, high-end for woodcock (U.S. EPA 2007b) Site Soil Conc mg/kg dw 9.785 Site

Dietary TRV mg/kgBW-d 4.53 Ueda et al. 2005, Japanese quail, chick mortality, 30 ppm dw p,p'DDT feed Conc Worm mg/kg ww 7.534 =BAF*Soil Conc Conc Plant mg/kg ww 0.289 =BAF*Soil Conc DF Veg mg/kg ww 0.5 Estimated mean DF Worm mg/kg ww 0.5 Estimated mean DF Soil mg/kg dw 0.020 Estimated Soil-Worm BAF ratio ww/dw 0.77 ww, site Soil -to-Plant BAF ratio ww/dw 0.0295 ww, site

Dose mg/kgBW-d 6.807 =(NIRww*Conc Worm*DFworm)+(NIRww*Conc Plant*Dfplant)+(NIRdw*Conc Soil*DFsoil) Soil PRG mg/kg dw 9.3 =TRV/(NIRww*BAFworm*DFworm)+(NIRww*BAFveg*DFveg)+(NIRdw*DFsoil)

CDM Method (Ueda et al. 2005, NOAEL, reproduction)

Dietary TRV mg/kgBW-d 0.84 Ueda et al. 2005, 6 ppm Soil PRG mg/kg dw 1.7 =TRV/(NIRww*BAFworm*DFworm)+(NIRww*BAFveg*DFveg)+(NIRdw*DFsoil)

PRG = LOAEL or NOAEL / SUM ((NIRww * BAFPrey1 * DFPrey1…x * SFF) + (NIRdw * DFsoil * SFF)) SFF - site foraging factor = 1.0

Effect - 40 % mortality of 0-14 d chicks with 4-5 weeks exposure to parental quail compared to 16-18 % mortality in control.

CDM Method (Mahoney LOAEL, 5-week fat accumulation)

NIR (Food) kg ww/kgBW-d 1.205 U.S. EPA 1993

NIR (Food) kg dw/kgBW-d 0.214 Eco-SSL, high-end for woodcock (U.S. EPA 2007b) Site Soil Conc mg/kg dw 9.785 Site

Dietary TRV mg/kgBW-d 5.2 Mahoney 1975, white-throated sparrow, 5-wk fat accumulation, 25ppm dw feed, technical DDT Conc Worm mg/kg ww 7.534 =BAF*Soil Conc Conc Plant mg/kg ww 0.289 =BAF*Soil Conc DF Veg mg/kg ww 0.5 Estimated mean DF Worm mg/kg ww 0.5 Estimated mean DF Soil mg/kg dw 0.020 Estimated Soil-Worm BAF ratio ww/dw 0.77 ww, site Soil -to-Plant BAF ratio ww/dw 0.0295 ww, site

Dose mg/kgBW-d 6.807 =(NIRww*Conc Worm*DFworm)+(NIRww*Conc Plant*Dfplant)+(NIRdw*Conc Soil*DFsoil) Soil PRG mg/kg dw 10.7 =TRV/(NIRww*BAFworm*DFworm)+(NIRww*BAFveg*DFveg)+(NIRdw*DFsoil)

CDM Method (Mahoney NOAEL, 5-week fat accumulation)

Dietary TRV mg/kgBW-d 1.04 Mahoney 1975, 5 ppm dw feed Soil PRG mg/kg dw 2.1 =TRV/(NIRww*BAFworm*DFworm)+(NIRww*BAFveg*DFveg)+(NIRdw*DFsoil)

PRG = LOAEL or NOAEL / SUM ((NIRww * BAFPrey1 * DFPrey1…x * SFF) + (NIRdw * DFsoil * SFF)) SFF - site foraging factor = 1.0

Effect - 48 % decrease in fat content at highest dose compared to control with 5-wk exposure Uncertainty - food ingestion rate not reported. There are no treatment differences in fat accumulation after 11 weeks exposure (Mahoney 1974). Technical DDT - 79 % p,p'-DDT and 21 % o,p'-DDT or p,p'-DDE (Mahoney 1975) (Reported statistically significant difference in weight gain at 5 weeks (Mahoney 1975) is not biologically meaningful - back-transformed difference of < 0.2 % between treatments and control. There were no statistically discernible weight differences in any of 5 subsequent measurement periods through 11 weeks, or any of 5 preceding measurement periods.)

CDM Method (Davison et al. 1976 LOAEL, reproduction)

NIR (Food) kg ww/kgBW-d 1.205 U.S. EPA 1993

NIR (Food) kg dw/kgBW-d 0.214 Eco-SSL, high-end for woodcock (U.S. EPA 2007b) Site Soil Conc mg/kg dw 9.785 Site

Dietary TRV mg/kgBW-d 5.2 Davison et al. 1976, Japanese quail, caged pair egg breakage, 40 ppm p,p'-DDT feed Conc Worm mg/kg ww 7.534 =BAF*Soil Conc Conc Plant mg/kg ww 0.289 =BAF*Soil Conc DF Veg mg/kg ww 0.5 Estimated mean DF Worm mg/kg ww 0.5 Estimated mean DF Soil mg/kg dw 0.020 Estimated Soil-Worm BAF ratio ww/dw 0.77 ww, site Soil -to-Plant BAF ratio ww/dw 0.0295 ww, site

Dose mg/kgBW-d 6.807 =(NIRww*Conc Worm*DFworm)+(NIRww*Conc Plant*Dfplant)+(NIRdw*Conc Soil*DFsoil) Soil PRG mg/kg dw 10.7 =TRV/(NIRww*BAFworm*DFworm)+(NIRww*BAFveg*DFveg)+(NIRdw*DFsoil)

CDM Method (Davison et al. 1976 NOAEL, reproduction)

Dietary TRV mg/kgBW-d 1.3 Davison et al. 1976, 10 ppm feed Soil PRG mg/kg dw 2.7 =TRV/(NIRww*BAFworm*DFworm)+(NIRww*BAFveg*DFveg)+(NIRdw*DFsoil)

PRG = LOAEL or NOAEL / SUM ((NIRww * BAFPrey1 * DFPrey1…x * SFF) + (NIRdw * DFsoil * SFF)) SFF - site foraging factor = 1.0

Effect - 27 % broken eggs at highest dose, 6-13 % breakage at lower doses and control (caged pairs) with 16-wk exposure Uncertainty - food ingestion rate not measured; moisture content not given for DDT concentration No difference in egg breakage with caged pairs of different strain of Japanese quail in smaller cages with 11-wk exposure

CDM Method (Cecil et al. 1978, LOAEL, survival)

NIR (Food) kg ww/kgBW-d 1.205 U.S. EPA 1993

NIR (Food) kg dw/kgBW-d 0.214 Eco-SSL, high-end for woodcock (U.S. EPA 2007b) Site Soil Conc mg/kg dw 9.785 Site

Dietary TRV mg/kgBW-d 22.7 Cecil et al 1978, chicken,adult survival, 500 ppm p,p'-DDT feed Conc Worm mg/kg ww 7.534 =BAF*Soil Conc Conc Plant mg/kg ww 0.289 =BAF*Soil Conc DF Veg mg/kg ww 0.5 Estimated mean DF Worm mg/kg ww 0.5 Estimated mean DF Soil mg/kg dw 0.020 Estimated Soil-Worm BAF ratio ww/dw 0.77 ww, site Soil -to-Plant BAF ratio ww/dw 0.0295 ww, site

Dose mg/kgBW-d 6.807 =(NIRww*Conc Worm*DFworm)+(NIRww*Conc Plant*Dfplant)+(NIRdw*Conc Soil*DFsoil) Soil PRG mg/kg dw 46.7 =TRV/(NIRww*BAFworm*DFworm)+(NIRww*BAFveg*DFveg)+(NIRdw*DFsoil)

CDM Method (Cecil et al. 1978, NOAEL, survival)

Dietary TRV mg/kgBW-d 2.27 Cecil et al 1978, 50 ppm feed Soil PRG mg/kg dw 4.7 =TRV/(NIRww*BAFworm*DFworm)+(NIRww*BAFveg*DFveg)+(NIRdw*DFsoil)

PRG = LOAEL or NOAEL / SUM ((NIRww * BAFPrey1 * DFPrey1…x * SFF) + (NIRdw * DFsoil * SFF)) SFF - site foraging factor = 1.0

Effect - 80 % mortality at highest dose, no mortality at next lowest dose or control Uncertainty - food ingestion rate not measured; moisture content not given for DDT concentration

CDM Method (Jeffries and French 1971, LOAEL, survival)

NIR (Food) kg ww/kgBW-d 1.205 U.S. EPA 1993

NIR (Food) kg dw/kgBW-d 0.214 Eco-SSL, high-end for woodcock (U.S. EPA 2007b) Site Soil Conc mg/kg dw 9.785 Site

Dietary TRV mg/kgBW-d 36 Jeffries and French 1971, pigeon, adult survival, p,p'-DDT Conc Worm mg/kg ww 7.534 =BAF*Soil Conc Conc Plant mg/kg ww 0.289 =BAF*Soil Conc DF Veg mg/kg ww 0.5 Estimated mean DF Worm mg/kg ww 0.5 Estimated mean DF Soil mg/kg dw 0.020 Estimated Soil-Worm BAF ratio ww/dw 0.77 ww, site Soil -to-Plant BAF ratio ww/dw 0.0295 ww, site

Dose mg/kgBW-d 6.807 =(NIRww*Conc Worm*DFworm)+(NIRww*Conc Plant*Dfplant)+(NIRdw*Conc Soil*DFsoil) Soil PRG mg/kg dw 74.1 =TRV/(NIRww*BAFworm*DFworm)+(NIRww*BAFveg*DFveg)+(NIRdw*DFsoil)

CDM Method (Jeffries and French 1971, NOAEL, survival)

Dietary TRV mg/kgBW-d 18 Jeffries and French 1971, pigeon Soil PRG mg/kg dw 37.0 =TRV/(NIRww*BAFworm*DFworm)+(NIRww*BAFveg*DFveg)+(NIRdw*DFsoil)

PRG = LOAEL or NOAEL / SUM ((NIRww * BAFPrey1 * DFPrey1…x * SFF) + (NIRdw * DFsoil * SFF)) SFF - site foraging factor = 1.0

Effect - 13 % mortality in highest dose treatment, no mortality in other treatments or control, 8-wk exposure