The Condor 86:383-389 0 The Cooper Omithologxal Society 1984

LEAD CONCENTRATIONS AND REPRODUCTION IN HIGHWAY-NESTING BARN SWALLOWS

CHRISTIAN E. GRUE THOMAS J. O’SHEA AND DAVID J. HOFFMAN

ABSTRACT. -Lead concentrationsin the carcassesand stomachcontents of adult and nestling Barn Swallows (Hirundo rustica) collected within the right-of-way of a major Maryland highway were greater than those found in Barn Swallowsnesting within a rural area. Lead concentrationsin the of adults from the highway colony were also greater than those of rural adults, but concentrations in the feathers of nestlingsfrom the two locations were similar. Activity of &aminole- vulinic dehydratase in red blood cells was lower in highway-nesting adults and their young than in their rural counterparts, although hemoglobin concen- trations and hematocrits did not differ. The number of ,nestlings, and body weights of the latter at 16-l 8 days of age were similar in the two colonies, as were body weightsof adults from the two areas.These resultssuggest that contamination of roadside habitats bv lead from automotive emissionsdoes not pose a serious hazard to that are aerial feeders.

Birds inhabiting highway rights-of-way (30.4 termine if reproduction in birds that are aerial million ha in the United States [Smith 19761) feeders is adversely affected by lead from mo- may be exposed to lead from automotive ex- tor vehicle emissions.We selectedBarn Swal- haust through inhalation or ingestion of con- lows for study because they frequently use taminated food or grit. Twenty-two to 58% of highway bridges and culverts as nest sites the lead emitted from motor vehicles (106- (Jacksonand Burchfield 1975, Barr 1979). The 1 18 thousand metric tons in the United States Parkway was selected as a study site because in 197 5 alone [Provenzano 19781) accumu- concentrationsof lead had been determined in lates in the soil or vegetation within highway soil and grass(Chow 1970), (Gish rights-of-way (Ward et al. 1975, Little and Wif- and Christensen1973, Beyer and Moore 1980), fen 1978). Accumulation varies with traffic and small mammals (Clark 1979) collected density (Wheeler and Rolfe 1979) and distance there. Analysesof stomachcontents and guano from the road surface(Little and Wiffen 1978, samplesfrom collected closeto this Park- Ward et al. 1979). Lead concentrationsas high way suggestedthat some speciesof flying in- as 6,835, 1,180, and 682 ppm dry weight have sectsin the area contained high concentrations been reported in soils, vegetation, and inver- of lead (Clark 1979). tebrates, respectively (Williamson and Evans 1972, Little and Wiffen 1978). METHODS Lead concentrationshave been measured in The Parkway colony was located beneath a urban and rural pigeons (Columba livia; e.g., bridge above the Patuxent River (39”4’10”N, Hutton 1980, Hutton and Goodman 1980, Ohi 76”49’53”W). According to the Maryland De- et al. 1981), doves (Siegfried et al. 1972) and partment of Transportation, the average daily songbirds(Getz et al. 1977). However, the ef- traffic volume (ADT) on the bridge in 1979 fects of this metal on their survival and repro- was 37,925 vehicles per day. The right-of-way duction have not been assessed,although di- was bordered by eastern deciduous forest; the etary concentrations of lead as low as 1 ppm median at each end of the bridge was covered reduced eggproduction in JapaneseQuail (Co- by short grass. The reference colony was lo- turnix coturnix japonica, Edens et al. 1976). cated in two adjacent barns on a small farm The objective of our study was to compare rural Howard County, Maryland lead concentrations, hematological parame- ;t9°12r50”N, 76”58’18”W), about 0.4 km from ters, and reproductive successin two colonies a lightly traveled secondaryroad (ADT = 330 of Barn Swallows(Hirundo rustica),one within vehiclesper day in 1979; Howard County Pub- the right-of-way of a major highway (Balti- lic Works). The surroundingsof the reference more-Washington Parkway), the other within colony were typical of colonies on farms in a nearby rural area (reference colony), to de- eastern Maryland, consistingof pasture, crop-

13831 384 C. E. GRUE, T. J. OSHEA’ AND D. J. HOFFMAN land (corn fields), and a large water impound- The entire plumage, bill, feet, and gastroin- ment. This colony was selectedas the reference testinal tract were removed from each speci- colony because of its accessibility, distance men. Stomach contents of nestlings in each from a major road, and similarity to the Park- colony were pooled for lead analysis;those of way colony in the number of nests present. adults in each colony were pooled by sex. During May, June, and July 1979, we mon- Stomach contentsand carcasseswere then fro- itored reproductive activity in the two colo- zen (- 15’C) until analyzed for lead. Feathers nies. Forty nests in each colony, containing (entire plumage) were thoroughly washed in first clutches,were checked every two days un- 0.1 % EastmanRTriton X- 100 (Eastman Ko- til hatching to determine clutch size, and dak Co., Rochester, NY) to remove lead par- checked again 16-18 days after the eggs ticles adsorbed to the surface. Remiges and hatched. At this time, nestlingswere counted rectriceswere cut into piecesto facilitate wash- and collected. Two were randomly selected ing. Featherswere mechanically agitated in the from each of 14-2 1 nests in each colony in surfactantfor 30 min, drained, and then rinsed order to determine the d-aminolevulinic acid thoroughly in deionized water. This process dehydratase(ALAD, E.C. 4.2.1.24) activity (a was repeated five times for each sample. (Mi- sensitive indicator of lead exposure in birds croscopic examination of selected samples of [Hoffman et al. 198 1, Ohi et al. 198 11) and feathersbefore and after washingindicated that hemoglobin content of red blood cells (RBC), the majority of the dirt particles had been re- hematocrits, and lead concentrationsin stom- moved.) Afterwards, feathers were dried in an ach contents, carcasses,and feathers (a lead oven at 90°C for 48 h. Samples of feathers, as accumulator [Nezel and Vogt 19761).To make well as carcassesand stomach contents, were our selection random, we removed entire then transferred to separate chemically-clean broods from their nests,assigned a number to bottles, weighed, dried for at least 48 h at 90°C each nestling within a brood, and chose the and then reweighed. Twenty milliliters of con- nestlingsto be sacrificedusing a random num- centrated HN03 was then added to each sam- ber table. The remaining nestlingswere anes- ple and it was allowed to stand for at least one thetized by placing them in a plastic bag with week with mixing at least once a day. Samples cotton lightly moistened with MetafaneR (Pit- were then transferredto 1OO-ml Kjeldahl flasks, man-Moore, Inc., Washington Crossing, NJ. additional HNO, was added, and the contents [Use of trade names or names of suppliers is reduced to a volume of 3 ml by heating. Car- for identification purposesonly and does not cassand sampleswere then diluted to constitute endorsement by the federal govern- 50 g with deionized water, whereas stomach ment.]), and returned to their nests.We anes- contents were diluted to 10 g. thetized the nestlings so that they would not Lead concentrations in stomach contents, fledgeprematurely when replacedin their nests. carcasses,and feathers were determined (by We tried to collect nestlingsat each colony on the Environmental Trace SubstancesResearch the same dates. After most of the young from Center, University of Missouri, Columbia) with these first clutcheshad fledged,we mist-netted a furnace-atomic absorption spectrophotom- 10-l 3 adults of each sex at each location to eter (Perkin-Elmer Model 403 with a HGA- determine the ALAD activity and hemoglobin 2 100 furnace) and an AS- 1 auto sam- content of RBCs, hematocrits, and lead con- pler. Background correction and the method centrations in the parts enumerated above. of standard additions were used. The lower We weighed all birds collected for blood and limit of reportable residuewas 0.0 1 ppm. High lead analyses and obtained a 4OOq.dblood values were checked by flame-atomic absorp- samplefrom each by decapitatingit. Blood tion spectrophotometry and agreement was sampleswere kept on ice prior to analyses.We satisfactory.Lead concentrations(ppm) are ex- determined ALAD activity in duplicate within pressedon a dry weight basisunless noted oth- 3 h of collection with methods described by erwise. Averages of lead concentrations are Burch and Siegel (1971), using 50 ~1 of blood presentedas geometric means becausethe data from nestlings because of their high ALAD were not normally distributed. levels, but 100 ~1 from adults. We defined a We netted an additional 23 adults from the unit of ALAD activity as the increase in ab- Parkway colony, individually color-marked sorbance (at 555 nm, 1.O-cm light path) per their feathers, and then releasedthem in order ml RBCs per h at 38°C. Hematocrits were de- to estimate the number of birds within the termined shortly after blood sampleswere col- colony that actually foraged within the right- lected using the microhematocrit method of-way. (Some swallowsfrom the Parkway col- (Davidsohn and Nelson 1974: 115). Additional ony had been seen foraging outside of the blood was used to determine hemoglobin con- right-of-way.) We observed swallowsfrom two centrations with the cyanomethemoglobin locations on each side of the Parkway, one on method (Hycel, Inc., Houston, TX). each side of the bridge, between 06:OO and

386 C. E. GRUE, T. J. OSHEA’ AND D. J. HOFFMAN

TABLE 3. Comparisonof reproductivesuccess of Barn lessor soft-shelledeggs by interfering with cal- Swallowsnesting within the right-of-way of theBaltimore- cium metabolism (e.g., Edenset al. 1976). Jap- WashingtonParkway and a nearbyrural area (reference colony)with that reported for othercolonies. anese Quail fed l-l 00 ppm lead experienced delayed sexual maturity, reduced fecundity,

Mean no. and lower hatchability of their eggs(Edens et Mean of youngProduc- No. of No. of clutch fledged/ tiv- al. 1976). Dietary concentrations of 500 ppm Reference nests eggslad sire “W ity (o/o) or more inhibited growth in several avian Parkwaycolony, 40 197 4.9 4.w 81.2 (e.g., Damron et al. 1969, Edens et al. 1979b 53 263 5.0 - - 1976). Levels of lead in the stomach contents Referencecolony, 40 181 4.5 1.3c 27.2 of our Parkway swallowswere, however, gen- 1979b 55 251 4.6 - - erally below those known to affect avian re- Barr(1979) 136 625 4.6 3.1 68.0 McGinnand Clark - - 4.7 - 76.3 production. Therefore, it is probably not sur- (1978)* prising that the clutch sizes,, and Altemus(1977) 61 4.4 3.6 96.1 body weights of Parkway adults, as well as the Snapp(1976) ” 3:: 1.750 4.7 3.5 74.2 body weights of their nestlings, were similar Samuel(1971) 94 ‘430 4.6 3.7 81.2 Mizuta(1963) 47 245 5.2 - - to those of birds from the reference colony or 65 - - 4.3 - other colonies of Barn Swallows (Table 3). Adams(1957Y 441 1,906 4.3 3.1 71.9 Subtle lead-induced physiological and behav- ’ Percentageof eggslad from which youngfledged. ioral abnormalities not detected in our study bFirst row = datafor nestsmonitored until the youngfledged, second TOW = data for all nestsin the colony. may nevertheless reduce the survival of ju- DNumber of 16 to l&day-old youngin nest. venile and adult swallowsin the Parkway col- d Includessecond clutches. ony. Lead exposure has been shown to alter nerve function (Hunter and Haigh 1977), levels 24 ppm for females; Table 2). Differences be- of brain enzymes (Dieter and Finley 1979), tween the sexes were not statistically signifi- behavior (Barthalmus et al. 1977), and the im- cant in either colony. Feathers of Parkway mune response(Truscott 1970) in birds. adultscontained about 20 times more lead than We found a 31-34% difference in the RBC feathers of their nestlings (range = 1.7-4.3 ALAD activity of adult Barn Swallows in the ppm), whereas those from adults in the ref- two colonies, and a 14% difference between erence colony contained about 10 times the levels in their nestlings. Although cadmium lead in feathers of their young (range = 1.4- and zinc also accumulate in roadside and ur- 5.4 ppm). However, the lead content of the ban environments (Gish and Christensen1973, feathers of nestlingsfrom the two colonies was Hutton and Goodman 1980) and inhibit RBC similar. ALAD activity, they only inhibit the activity Reproductive successin the Parkway colony of this enzyme at levels 1O-l 00 times those of was similar to that reported for other colonies lead (Davis and Avram 1978). Low concen- of Barn Swallows(Table 3). However, the pro- trations of cadmium and zinc actually stimu- ductivity of the reference colony was unusually late ALAD activity in RBCs (Davis and Avram low, owing to predation of eggsand nestlings 1978). Since concentrations of lead in soils in the barns. Body weights of adults and 16- within the right-of-way of the Parkway were to 1g-day-old nestlingsfrom the Parkway were as much as 440 times that of cadmium and similar to those of their rural counterparts(Ta- three times that of zinc in 1970 (Gish and ble 4). Nestlingswere significantlyheavier than Christensen 1973), the differenceswe noted in the adults in both colonies. RBC ALAD activity between the two colonies probably resulted from differencesin the birds’ DISCUSSION exposure to lead, and not other metals. Results of the blood and lead analysesfor the We do not know the biological implications two colonies of Barn Swallows indicate that of the differences in the RBC ALAD activity the lead intake (dietary and respiratory) of we found between the two swallow colonies. Parkway adults and nestlingswas greater than This enzyme is necessaryfor the synthesisof that of their rural counterparts. However, we heme, which is incorporated into hemoglobin did not observe any overt signs of lead poi- within erythrocytes and into mitochondrial cy- soning(e.g., weight loss, paralysisin wings and tochromes (Sassa et al. 1975). Inhibition of legs,or lossof vision; Osweiler and Van Gelder ALAD in cells of critical organs could jeop- 1978) in swallows from the Parkway colony. ardize metabolic and detoxifying processes Nor did we detect any impairment of repro- (Sassaet al. 1975). However, the difference in duction similar to that reported in other avian RBC ALAD that we observed was not as pro- speciesexposed to lead under laboratory con- nounced as that reported in birds in which ditions. For example, dietary lead has de- other lead-induced physiological abnormali- creasedeggshell quality and resulted in shell- ties have occurred. For example, the activity LEAD AND REPRODUCTION IN SWALLOWS 387

TABLE 4. Body weights (g) of Barn Swallows from within the right-of-way of the -Washington Parkway and a nearby rural area (reference).Values in the table are x i SD (n).*

Ase Sex Parkwaycolony Referencecolony Adult Male 17.9 f 0.6 (lO)a 17.8 f 1.1 (lO)a Adult Female 18.8 + 1.1 (13)a 18.0 + 1.8 (lO)a Nestlings** - 19.5 f 1.2 (21)b 19.5 + 1.2 (14)b

* Valuesfollowed by differentletters differ significantly(P -C0.05, two-wayANOVA wth Bonfermni mean separation). ** Eachobservation (n,) is the averageweight for two 16- to IS-day-old nestlingsrandomly selected from eachnest in the sample(n)

of RBC ALAD diminished 75% in Mallard pean Starlings (Sturnus vulgaris) from nest ducks (Anus plat~~%~~~cho.s)after ingestion of boxes within the median of the Parkway (84- lead shot; nerve cell damage in brain tissue 94 ppm; C. E. Grue, unpubl. data) support this was apparent (Dieter and Finley 1979). It de- conclusion. Furthermore, the stomach con- clined 80% in Bald Eagles (Huliaeetus leuco- tents of bats (Eptesicusfuscus and Myotis lu- cephalus)that ingestedlead shot; hematocrits czfig~s) believed to forage within the right-of- and hemoglobin concentrations were reduced way of this Parkway contained lead concen- 20-25%, and changesin serum chemistry in- trations (3.8-26 ppm wet weight) that were dicated that the birds’ kidneys and livers were considerably lower than those of shrews (240 damaged (Hoffman et al. 198 1). Four of the ppm wet weight) collected in the same area five eagles eventually died, and the fifth be- (Clark 1979), but greater than comparable val- came blind; cardiovascular and renal lesions uesfor the adult Parkway swallowsin our study attributable to lead poisoning were present in (1.0-1.9 ppm wet weight). the birds at necropsy (Pattee et al. 198 1). The Concentrations of lead in carcasses and activity of the enzyme was inhibited 96% in feathers were higher in Barn Swallows from pigeons from downtown London, as was that the Parkway than in the reference group. Sim- of succinate dehydrogenase in their kidneys ilar results have been reported for these and (67%) and livers (33%; Hutton 1980). Results other parts of birds inhabiting urban areas, of these studies and the absenceof detectable highway rights-of-way, and other areas con- differences in hemoglobin and hematocrit taminated with lead (e.g., Getz et al. 1977? levels in the two populations in the present Hutton 1980, Hutton and Goodman 1980, Ohi study suggestthat the differences among the et al. 198 1; for an exception, see Udevitz et latter were not biologically significant. al. 1980). To our knowledge, the only other Lead concentrations(ppm dry weight) in the study in which lead concentrations in avian stomach contents of Barn Swallows from the carcassesare reported as we have done is that Parkway colony (3.2-6.8) were generally lower of White et al. (1977), who found that urban than those found in invertebrates collected ad- EuropeanStarlings contained a geometricmean jacent to highways: earthworms, for example, (GM) of 0.89 ppm lead on a wet weight basis. contained 26-500 ppm, woodlice 380-682, Lead concentrations (ppm wet weight) in car- 43-82, ants 15-45, 9-16, cassesof adult Barn Swallows from the Park- grasshoppers3.4-3.8, tent caterpillars 7.1-7.4, way colony (GM = 1.9 ppm for males and 3.5 mantids 4-l 5, damsel 8-9, suckinginsects ppm for females) were two to four times greater 10-16, chewing insects 10-27, and predatory than this value. insects 20-31 (Williamson and Evans 1972, Lead concentrations in carcassesof female Giles et al. 1973, Gish and Christensen 1973, Barn Swallows from both colonies exceeded Price et al. 1974, Goldsmith and Scanlon 1977, those in the carcassesof males, but these dif- Ash and Lee 1980, Beyer and Moore 1980, ferenceswere not statistically significant. Such Robe1et al. 198 1). Terrestrial invertebrates ap- differencesbetween sexeshave, however, been parently accumulate lead in proportion to their reported in other speciesof birds (Finley et al. proximity to the soil and the amount of soil 1976, Finley and Dieter 1978, Hutton and or litter that they ingest. Lead concentrations Goodman 1980, Kendall and Scanlon 1981) are highest in and lowest in her- and small mammals (e.g., Clark 1979). In birds, bivorous insects.Birds, suchas Barn Swallows, the differencesappear to be associatedwith the which feed on small flying insects would be increasedcalcium requirement of females dur- expected to accumulate less dietary lead than ing -laying, because lead accumulation in birds and small mammals that feed on terres- bone is enhanced by mobilization trial invertebrates. Comparison of lead con- (Finley et al. 1976, Finley and Dieter 1978). centrations (ppm dry weight) in stomach con- That female birds accumulate more lead in tents of Barn Swallows from the Parkway their bones than males may explain why lead colony with those in adult and nestling Euro- concentrations in the feathers of male Barn 388 C. E. GRUE, T. J. OSHEA’ AND D. J. HOFFMAN

Swallows exceeded those of females in both and L. M. Thomas for secretarialassistance. Critical re- colonies. views by W. N. Beyer, C. Lewis, R. A. Lewis, W. E. Odum, Concentrations of lead in the feathers of ru- and 0. H. Pattee improved the manuscript. ral adult Barn Swallows (Table 2) were similar LITERATURE CITED to those found in the feathers of ground-for- ADAMS,L. E. G. 1957. Nest recordsofthe swallow. Bird aging songbirdsfrom rural areas (X = 6.4-36 Study 428-33. ppm; Getz et al. 1977). However, lead con- ALTEMUS,E. L. 1977. nesting data. Cas- centrations in feathers of adult swallows from sinia 56~24-25. the Parkway colony were about three times ASH, C. P. J., AND D. L. LEE. 1980. Lead, cadmium, those of adults from the reference colony, copper and iron in earthworms from roadside sites. Environ. Pollut. Ser. A 22~59-67. whereas concentrations in feathers of urban BARR,A. L. 1979. Nesting success,growth rates, and ground-foraging songbirds were about 3-35 recruitment of Barn Swallows (Hirundo rustica) in times those of their rural counterparts (Getz Brazos County, Texas. M.Sc. thesis. Texas A&M et al. 1977). These data support the hypothesis Univ., College Station. that birds which forage on the ground are ex- BARTHALMUS,G. T., J. D. LEANDER,D. E. MCMILLAN, P. MUSHAK,AND M. R. KRIGMAN. 1977. Chronic ef- posed to more lead than aerial feeders. Our fects of lead on schedule-controlledpigeon behavior. finding that lead levels in tissues of nestling Toxicol. Appl. Pharmacol. 42:27 l-284. Barn Swallows from both colonies were ‘/6- BEYER,W. N., AND J. MOORE. 1980. Lead residues in l&h of those found in adults indicates that eastern tent caterpillars (MuZucosomaamericanurn) and their host plant (Prunes serotinn)close to a major lead is present in nestlings from colonies in highway. Environ. Entomol. 9: 10-12. both contaminated and uncontaminated sites, BURCH,H. B., AND A. L. SIEGEL.197 1. Improved method and that it accumulates in tissuesover time. for measurement of delta-aminolevulinic acid dehy- A similar conclusion was reached by Tansy dratase activity in human erythrocytes. Clin. Chem. 17:1038-1041. and Roth (1970) for urban pigeons. CHOW,T. J. 1970. Lead accumulation in roadside soil Concentrations of lead in the carcasswere and grass.Nature 225:295-296. about 15 times greater in the bats that appar- CLARK,D. R., JR. 1979. Lead concentrations:bats vs. ently foraged on flying insectsabove the Park- terrestrial small mammals collected near a major way right-of-way (GM = 32-47 ppm wet highway. Environ. Sci. Technol. 13:338-34 1. DAMRON,B. L., C. F. SIMPSON,AND R. H. HARMS. 1969. weight; Clark 1979) than in adult Barn Swal- The effect of feeding various levels of lead on the lows in the same area. Several factors may performance of broilers. Poult. Sci. 48: 1507-l 509. account for this difference. Bats, for example, DIETER,M. P., AND M. T. FINLEY. 1979. &aminolevu- fed on insectsthat contained 4-l 3 times more linic acid dehydrataseenzyme activity in blood, brain and liver of lead dosed ducks. Environ. Res. 19:127- lead than those consumed by our swallows. 135. Differences in prey, physiology, and the du- DAVIDSOHN,I., AND D. A. NELSON. 1974. Blood, p. 1OO- ration of lead exposure may also have been 347. In I. Davidsohn and J. B. Henry [eds.], Clinical important. Futhermore, the use of unleaded diagnosis by laboratory methods. W. B. Saunders, gasolineincreased between 1976, when the bats Philadelphia. DAVIS,J. R., AND M. J. AVRAM. 1978. A comparison of were studied,and 1979, when we did our study. the stimulatory effects of cadmium and zinc on nor- Differences in the accumulation of lead by hair mal and lead-inhibited erythrocytic &aminolevulinic and feathers may also have been a factor, as acid dehydratase activity in vitro. Toxicol. Appl. may the fact that Barn Swallows molt twice a Pharmacol. 44:181-190. year, whereas bats appear to molt only once EDENS,F. W., E. BENTON,S. J. BURSIAN,AND G. W. MOR- GAN. 1976. Effect of dietary lead on reproductive (Quay 1970). performancein JapaneseQuail, Coturnix coturnixju- Our resultssuggest that lead from motor ve- ponicu. Toxicol. Appl. Pharmacol. 38:307-314. hicle emissionsdoes not pose a serioushazard FINLEY,M. T., AND M. P. DIETER. 1978. Influence of to birds that feed on flying insectswithin high- laying on lead accumulationin bone of Mallard ducks. J.-Toxicol. Environ. Health 4: 123-129. way rights-of-way. Comparable data for FINLEY.M. T.. M. P. DIETER.AND L. N. LOCKE. 1976. ground-feedingbirds are needed to adequately Lead in tissuesof Mallard’ducks dosedwith two types assessthe effects of lead from motor vehicles oflead shot. Bull. Environ. Contam. Toxicol. 16:261- on birds inhabiting these areas. 268. GETZ, L. L., L. B. BEST,AND M. PRATHER. 1977. Lead ACKNOWLEDGMENTS in urban and rural song birds. Environ. Pollut. 12: 235-238. We thank J. E. Spaine and the National Park Service for GILES,F. E., S. G. MIDDLETON,AND J. G. GRAU. 1973. allowing us to work on their lands, and M. D. Wallace Evidence for the accumulation of atmospheric lead and J. K. Solem for help in locating the referencecolony: by insects in areas of high traffic density. Environ. C. W. Birdsall, C. L. Bratch, C. L. Christian, N. L. Glad: Entomol. 2:299-300. son, C. H. Gorsuch, and B. E. Keves. who helned monitor GISH, C. D., AND R. E. CHRISTENSEN.1973. Cadmium, reproductive activity in the two-colonies: and S. S. Os- nickel, lead, and zinc in earthworms from roadside borne, who assisted-with the blood assays:We also thank soil. Environ. Sci. Technol. 7:1060-1062. M. C. Perry for preparingthe feather dyes, T. A. Grunwald GOLDSMITH,C. D., JR., AND P. F. SCANLON.1977. Lead and G. L. Hensler for help with the statistical analyses, levels in small mammals and selected invertebrates LEAD AND REPRODUCTION IN SWALLOWS 389

associatedwith highwaysof different traffic densities. nants,graphic patterns and future trends.J. Air Pollut. Bull. Environ. Contam. Toxicol. 17:31l-3 16. Control Assoc. 28: 1193-l 199. HOFFMAN,D. J., 0. H. PATTEE,S. N. WIEMEYER,AND B. QUAY, W. B. 1970. Integument and derivatives, p. l- MULHERN. 1981. Effects of lead shot ingestion on 56. In W. A. Wimsatt ted.], Biology of bats. Vol. 2. &aminolevulinic acid dehydrataseactivity: hemoglo- Academic Press, New York. bin concentration. and serum chemistrv in Bald Ea- ROBEL,R. J., C. A. HOWARD,M. S. UDEVI~Z, AND B. gles. J. Wildl. Dis. 17:423-431. C~RNETTE,JR. 1981. Lead contamination in vege- HUNTER,B., AND J. C. HAIGH. 1977. Case report-de- tation, cattle dung, and dung beetlesnear an interstate myelinating peripheral neuropathy in a Guinea Hen highway, Kansas. Environ. Entomol. 10:262-263. associatedwith subacutelead intoxication. Avian Dis. SAMUEL,D. E. 1971. The breeding biology of Barn and 221344-349. Cliff swallowsin West Virginia. Wilson Bull. 83:284- HUTTON,M. 1980. Metal contamination of feral pigeons 301. Columba livia from the London area: part 2 - biolog- SASSA,S., S. GRANICK,AND A. KAPPA. 1975. Effects of ical effects of lead exposure. Environ. Pollut. Ser. A lead and genetic factors on heme biosynthesisin the 22128l-293. human red blood cell. Ann. N.Y. Acad. Sci. 244:419- HUTTON?M., AND G. T. GOODMAN. 1980. Metal con- 440. tamination of feral pigeons Columba livia from the SIEGFRIED,W. R., P. G. H. FROST,E. P. REDELINGHUYS, London area: part 1-tissue accumulation of lead, AND R.P. VAN DERMERWE. 1972. Lead concentra- cadmium and zinc. Environ. Pollut. Ser. A 22:207- tions in the bones of city and country doves. S. Afr. 217. J. Sci. 68:229-230. JACKSON,J. A., ANDP. G. BURCHFIELD.1975. Nest-site SMITH, W. 1976. Lead contamination of the roadside selectionofBarn Swallowsin east-centralMississippi. ecosystem._J.Air Pollut. Control Assoc. 26:753-766. Am. Midl. Nat. 94:503-509. SNAPP,B. D. 1976. 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