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Patterns of organochlorine pesticide contamination in Neotropical migrant passerines in relation to diet and winter habitat
Chemosphere 41 (2000) 1107±1113
Patterns of organochlorine pesticide contamination in Neotropical migrant passerines in relation to diet and winter habitat J.A. Klemens
a,1
, R.G. Harper a, J.A. Frick b,*, A.P. Capparella c, H.B. Richardson a, M.J. Coey d
a Department of Biology, Illinois Wesleyan University, Bloomington, IL 61702-2900, USA Department of Chemistry, Illinois Wesleyan University, P.O. Box 2900, Bloomington, IL 61702-2900, USA c Ecology Group, Department of Biological Sciences, Illinois State University, Normal, IL 61790-4120, USA U.S. Fish and Wildlife Service, Rock Island Field Oce, 4469 48th Avenue Court, Rock Island, IL 61201-9213, USA b
d
Received 19 February 1999; accepted 19 July 1999
Abstract Eleven species of Neotropical migrant passerines collected in Illinois (USA) during May 1996, were analyzed for the presence of organochlorine (OC) pesticides. At least one of ®ve OC pesticide residues was detected in 66 of 72 birds, representing all species examined. The contaminants most frequently detected were p; p0 -DDE, dieldrin and heptachlor epoxide, all of which were present in the 10±30 ng/g range. Insectivores had signi®cantly higher levels of these compounds than did non-insectivores, while there was no signi®cant main eect of winter habitat (forest and scrub). Future research on OC pesticide contamination in resident New World passerines may allow more accurate predictions regarding the sources of contamination in Neotropical migrants. Ó 2000 Elsevier Science Ltd. All rights reserved. Keywords: Organochlorine; Neotropical migrant; Passerine; Pesticide; Diet; Winter habitat
1. Introduction Migratory birds can accumulate pesticides over vast geographic areas (Gard et al., 1995). Over the past decade there has been much interest in pesticide contamination in Neotropical migrant passerines (songbirds that winter in the Caribbean, Mexico and Central and South America, but breed in the United States and Canada). Some Neotropical migrant passerines are believed to be
* Corresponding author. Tel.: +1-309-556-3159; fax: +1-309556-3864. E-mail address: [email protected] (J.A. Frick). 1 Present address: Department of Biology, Leidy Labs, University of Pennsylvania, Philadelphia, PA 19104-6018, USA.
in decline (Robinson, 1997), and organochlorine (OC) pesticide contamination has been suggested as a possible cause for these declines (Gard et al., 1993, 1995; Block et al., 1995). However, there is a paucity of data on the extent to which Neotropical migrant passerines are exposed to such pesticides (Harper et al., 1996). The collection of baseline data is an appropriate ®rst step in evaluating the eects of pesticides on the population dynamics of Neotropical migrants (Gard et al., 1993). The purpose of this study was to document OC pesticide contamination levels in species of Neotropical migrant passerines for which few baseline data exist, and to look for patterns of contamination in relation to diet and winter habitat preferences. Analysis of diet in relation to OC contamination levels is important because insectivores may be at greater risk than non-insectivores to accumulate substantial pesticide burdens (Gard et al.,
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J.A. Klemens et al. / Chemosphere 41 (2000) 1107±1113
1995), because they are at a higher trophic level. Annually, many species of Neotropical migrants spend the greatest amount of time on their Latin American wintering grounds compared to the time spent on their breeding grounds and during migration (Keast, 1980). OC pesticides continue to be used in parts of Central and South America (Rapaport et al., 1985; Standley and Sweeney, 1995; Mora, 1997). Winter habitat preferences of Neotropical migrant passerines may indicate the relative proximity of the birds to possible sources of contamination. For example, scrub habitat that develops after forests are cleared are sometimes close to land used for agricultural purposes in the Neotropics (Capparella, pers obs), and birds that winter in such habitat may more likely be exposed to OC pesticides. 2. Methods 2.1. Collection and preparation of birds Seventy-two Neotropical migrants were either salvaged as television tower kills (N 13) or collected in mist nets (N 59). Tower kills were collected on 16 May 1996 in Livingston County, IL, USA (40° 520 , 88° 330 ). Mist netting was conducted from 14 May 1996 to 22 May 1996 at the Keithsburg Division of the Mark Twain National Wildlife Refuge in Mercer County, IL, USA (41° 060 , 90° 570 ). The birds were put on ice or dry ice at the time of collection and were later transferred to a ÿ80°C freezer for storage until they were thawed and prepared as museum skin specimens (Frick et al., 1998). The museum skins were deposited in the Illinois State University Department of Biological Sciences bird collection. The skinning procedure resulted in the skin, feathers, distal limbs, bill, partial braincase and stomach being excluded from analysis. All other parts of the carcass were included in the analysis, although the contents of the digestive tract were rinsed with distilled water in order to prevent contamination by recently ingested materials. Care was taken to remove all visible subcutaneous fat from the skins, and this fat was included in the pesticide analysis. All birds used in this study were classed as ``After Hatch Year'' (AHY), which was based upon the US Fish and Wildlife Service Bird Banding Laboratory method of assigning all individuals collected after 1 January, but before the breeding season, as AHY. After preparing the study skin, the carcass was refrozen until chemical analyses could be performed. 2.2. Residue analysis Analyses were performed using gas chromatography (Frick et al., 1998). The chemicals assayed for were aldrin, 2,2-Bis(4-chlorophenyl)-1,1-dichloroethane
(p,p0 -DDD), 2,2-Bis(4-chlorophenyl)-1,1-dichloroethylene (p,p0 -DDE), 2,2-Bis(4-chlorophenyl)-1,1,1-trichloroethane (p,p0 -DDT), dieldrin, endosulfan I, endosulfan II, endosulfan sulfate, endrin, endrin aldehyde, heptachlor, heptachlor epoxide, alpha-hexachlorocyclohexane, beta-hexachlorocyclohexane, delta-hexachlorocyclohexane, lindane, and methoxychlor. Detection limits were 0.01 lg for all pesticides except the following: heptachlor (0.02 lg), aldrin (0.03 lg), endosulfan I (0.03 lg) and endosulfan sulfate (0.10 lg). Levels of OC pesticides in duplicate samples were within ®ve percent of each other. 2.3. Statistical analysis Only p,p0 -DDE, dieldrin, and heptachlor epoxide were found in a sucient number of carcasses for statistical analyses. All concentrations that were below detection limits were treated as zeros. Mean pesticide levels were calculated for all 11 species and were used in the following analyses because of the variable sample sizes among species (see Table 1). These means were then log transformed to meet the assumption of normality. Birds were categorized according to diet (i.e. insectivore and non-insectivore) based on their primary diet during the breeding season (Ridgely and Tudor, 1989; Payne, 1992; Rappole et al., 1993; Briskie, 1994; Curson et al., 1994; Ridgely and Tudor, 1994; DeGraaf and Rappole, 1995; Kricher, 1995; McCarty, 1996; Stotz et al., 1996; Lanyon, 1997). Winter habitat preferences (i.e. forest and scrub) were taken from previous studies (Waide, 1980; Robbins et al., 1989). Diet and winter habitat preferences were analyzed with two-way ANOVA (Sokal and Rohlf, 1995) independently for each of the three compounds listed above, using SPSS software (Norusis, 1993). One-way ANOVA (Sokal and Rohlf, 1995) was used when interaction terms were signi®cant. Data reported are untransformed means and upper 95% con®dence limits (Sokal and Rohlf, 1995). 3. Results At least one of ®ve OC pesticide residues was detected in 66 of 72 birds, representing all species examined (Table 1). In addition to the most frequently detected compounds in Table 1, ®ve birds also contained p,p0 -DDT and four birds contained p,p0 -DDD. Six individuals of four species contained OC levels below detection limits. Insectivores contained signi®cantly higher levels of p,p0 -DDE, dieldrin, and heptachlor epoxide than did non-insectivores (Tables 2 and 3). There was no significant main eect of winter habitat type on levels of p,p0 DDE, dieldrin, and heptachlor epoxide. The interaction between diet and winter habitat type was not signi®cant
b
Number contaminated. Con®dence limit. c Insectivore. d Forest winter habitat. e Scrub winter habitat. f Non-insectivore.
a
c; d
Great-crested Flycatcher (Myiarchus crinitus) Least Flycatcherc;e (Empidonax minimus) Eastern Wood Peweec;e (Contopus virens) Swainson's Thrushf ;d (Catharus ustulatus) Warbling Vireoc;d (Vireo gilvus) Black-and-white Warblerc;d (Mniotilta varia) Prothonotary Warblerc;d (Protonataria citrea) Yellow Warblerc;e (Dendroica petechia) Common Yellowthroatc;e (Geothlypis trichas) Rose-breasted Grosbeakf;e (Pheucticus ludovicianus) Indigo Buntingf;e (Passerina cyanea)
Species
6 10 3 7
6 10 5 10
11.74 + 9.31
1.36 + 2.49
251.67 + 443.00 391.43 + 791.69
4.94 + 3.46 39.40 + 26.26 20.85 + 141.67 4.57 + 3.10 53.20 + 53.66 70.94 + 36.06 4.40 + 35.28
5
3
6 8
2 5 1 6 5 7 5
NC
4 5 2 7 5 10 5
Dieldrin
NCa
x 95% CLb
p,p0 -DDE
Levels of OC contaminants (ng/g)
5 5 2 9 5 10 5
N
3.07 + 3.20
1.80 + 4.12
60.00+63.46 15.86 + 8.33
2.84 + 4.91 38.80 + 11.36 22.00 + 279.54 8.48 + 7.65 15.04 + 8.04 18.90 + 12.42 15.20 + 10.77
x 95% CL
Table 1 Means and upper 95% con®dence limits of the most frequently detected OC contaminants in Neotropical migrant passerines
1
2
4 7
2 5 1 6 3 8 5
0.17 + 0.37
0.57 + 1.28
27.17 + 29.45 14.95 + 8.79
2.28 + 3.88 25.60 + 9.23 12.50 + 158.83 4.89 + 4.24 11.60 + 14.20 12.54 + 7.08 13.58 + 6.82
x 95% CL
Heptachlor epoxide NC
J.A. Klemens et al. / Chemosphere 41 (2000) 1107±1113 1109
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J.A. Klemens et al. / Chemosphere 41 (2000) 1107±1113
Table 2 Results of two-way analysis of variance of most frequently detected OC levels in relation to diet and winter habitat type of Neotropical migrant passerines Eect
Compounda p,p0 -DDE
Diet Winter habitat type Diet ´ winter habitat type a
Dieldrin
Heptachlor epoxide
F
P
F
P
F
P
6.97 0.28 0.45
0.03 0.61 0.53
7.61 0.06 5.42
0.03 0.82 0.05
22.17 3.81 13.39
0.002 0.09 0.008
df 1; 7 for all entries.
Table 3 Mean and upper 95% con®dence limits of OC contamination levels for Neotropical migrant passerines in relation to diet and winter habitat Category
Na
Levels of OC contaminants (ng/g) Dieldrin
Diet Insectivores Non-insectivores Winter habitat Forest Scrub a b
Heptachlor epoxide b
x 95% CL
x 95% CL
8 3
23.58 + 14.87 4.45 + 8.81
15.03 + 6.69 1.87 + 6.50
5 6
12.09 + 7.94 23.59 + 23.54
8.98 + 6.28 13.49 + 12.25
The same species were categorized according to diet and winter habitat. Con®dence limit.
for p,p0 -DDE; however, it was signi®cant for dieldrin and highly signi®cant for heptachlor epoxide. For insectivores there were no signi®cant dierences in contamination levels of dieldrin in forest and scrub habitats F1;6 3:91; P 0:10, and heptachlor epoxide in forest and scrub habitats F1;6 3:21; P 0:12. However, for birds that winter in scrub habitat, insectivores had signi®cantly higher levels of dieldrin (x 34:16 65:62 ng/ g) compared to non-insectivores (x 2:43 10:46 ng/g; F1;4 29:07; P 0:006). Likewise, insectivores that winter in scrub habitat also had signi®cantly higher levels of heptachlor epoxide (x 20:05 31:84 ng/g) than did non-insectivores (x 0:37 2:92 ng/g; F1;4 75:40; P 0:001). 4. Discussion These ®ndings demonstrate that OC pesticide contamination is ubiquitous in the Neotropical migrant passerines examined in our study. These results were consistent with a recent study (Harper et al., 1996) in regard to both frequency of occurrence and level of contamination. Levels of contamination ranged across six orders of magnitude, while average levels were lower than those reported in other studies (DeWeese et al., 1986; Baril et al., 1990; Fyfe et al., 1990; Mora and Anderson, 1991). This study and another study (Harper
et al., 1996) provide a baseline level of pesticide contamination for Neotropical migrant passerines utilizing the Mississippi River ¯yway. The presence of higher levels of OC contamination in insectivores than in non-insectivores is not surprising, since insectivores occupy a higher trophic level than do non-insectivores. Similar results at these and higher levels (in the lg/g range) have been found in studies of other passerine and non-passerine species (Enderson et al., 1982; DeWeese et al., 1986; Fyfe et al., 1990). Insectivorous Neotropical migrant passerines may thus be at higher risk for possible deleterious eects from OC pesticides than non-insectivores. There was no eect of winter habitat on OC contamination levels. Neotropical scrub habitats that develop after forests are cleared are sometimes in close proximity to land used for agricultural purposes. Therefore, we predicted that scrub birds would have higher OC levels than forest birds, but this was not observed. It is possible that the birds in our sample winter in naturally occurring scrub habitat that may not be in close proximity to agricultural lands. The lack of signi®cant main eect of winter habitat and the signi®cant interaction of diet and habitat type for dieldrin and heptachlor epoxide may possibly be explained by the small sample size of non-insectivorous birds in this study (one species, Catharus ustulatus) that winter in scrub habitats.
J.A. Klemens et al. / Chemosphere 41 (2000) 1107±1113
With baseline data indicating that OC pesticide contamination is common in Neotropical migrant passerines, future research on this topic should focus on two major areas. The ®rst is determining what, if any, deleterious eects low-level OC pesticide contamination has on passerines. Organochlorine contaminants have been shown to aect avian reproduction in subtle but potentially disastrous ways (Colburn et al., 1993), but little toxicological research has explicitly focused on passerines (Gard et al., 1993). What remains to be determined is if contamination at the levels detected in this study will lead to reproductive problems in these passerines. Other studies on passerines have documented no apparent eects on reproductive success in passerines with OC compounds in the lg/g range. Elliott et al. (1994) found no reproductive eects in a population of American robins (Turdus migratorius) with eggs contaminated with p,p0 -DDE at levels of 80 lg/g. Custer et al. (1998) found that the concentration of polychlorinated biphenyls (PCBs) of up to 10 lg/g in tree swallow (Tachycineta bicolor) eggs did not seem to aect hatching success. Bishop et al. (1999) found no eect on hatching success or ¯edging rates of tree swallows contaminated with p,p0 -DDE and PCBs at levels up to 11.1 lg/g. In contrast, McCarty and Secord (1999) documented reduced nest quality, a trait correlated with lower reproductive success, in tree swallows contaminated with PCBs in the 5±25 lg/g range. However, none of these studies investigated possible multigenerational eects of these OC compounds, whose eects can also vary among species (Colborn and Clement, 1992). The second area future research should address is determining the sources of OC pesticide contamination, which may also have conservation implication for raptorial birds that feed upon passerines. Neotropical migrant passerines may acquire OC compounds on their Neotropical wintering grounds, where OC pesticides may still be widely used (Rapaport et al., 1985; Standley and Sweeney, 1995; Mora, 1997). Migrants may also acquire them in the Nearctic, where many OC pesticides have been banned, but have been historically applied in great quantities (DeWeese et al., 1986). A third possibility is that Neotropical migrants may be exposed to OC compounds on feeding stops during migration. Migrating birds often stop to rebuild fat reserves, which can result in increases in body mass of up to 10% in a single day (Moore and Kerlinger, 1990; Moore and Simons, 1992). The pesticides documented in this study may be acquired at such feeding stops and may not represent levels acquired over long periods of time. However, it should be noted that OC levels may in fact represent accumulation from more than one of these sources. Organochlorine pesticide ``hotspots'' still exist in many parts of the Nearctic and Neotropics (Simonich and Hites, 1995; Blais et al., 1998). In Mexico DDT is applied to control outbreaks of malaria (Mora, 1997),
1111
while the current usage of dieldrin and heptachlor is unknown. Comparison of OC contamination in resident passerine avifaunas throughout the new world with those levels encountered in Neotropical migrant passerines may allow more accurate predictions regarding the sources of OC contamination. Acknowledgements We thank the National Science Foundation (BIR9601523) for support to purchase the gas chromatograph, and Illinois Wesleyan University for partial support of this work through an Artistic and Scholarly Development Grant to Harper and Frick. A. Bartuszevige, V. Flanagin, N. Laurie and M. Wieland assisted with pesticide extraction, and S. Janota and F. Hollingworth assisted with collection of specimens. S. Soukup, J. Hu and two anonymous reviewers made helpful suggestions that improved the manuscript. References Baril, A., Elliott, J.E., Somers, J.D., Erickson, G., 1990. Residue levels of environmental contaminants in prey species of the peregrine falcon, Falco peregrinus, in Canada. Can. Field-Nat. 104, 273±284. Bishop, C.A., Mahony, N.A., Trudeau, S., Pettit, K.E., 1999. Reproductive success and biochemical eects in tree swallows (Tachycineta bicolor) exposed to chlorinated hydrocarbon contaminants in wetlands of the Great Lakes and St. Lawrence River basin, USA and Canada. Environ. Toxicol. Chem. 18, 263±271. Blais, J.M., Schindler, D.W., Muir, D.C.G., Kimpes, L.E., Donald, D.B., Rosenberg, B., 1998. Accumulation of persistent organochlorine compounds in mountains of western Canada. Nature 395, 585±588. Block, W.M., Finch, D.M., Brennan, L.A., 1995. Single-species versus multiple-species approaches for management. In: Martin, T.E., Finch, D.M. (Eds.), Ecology and Management of Neotropical Migratory Birds: a Synthesis and Review of Critical Issues. Oxford University Press, Oxford, pp. 461±476. Briskie, J.V., 1994. Least ¯ycatcher (Empidonax minimus). In: Poole, A., Gill, F. (Eds.), The Birds of North America, vol. 99, The Academy of Natural Sciences, Philadelphia, Pennsylvania and The American OrnithologistsÕ Union, Washington, D.C. Colborn, T., Clement, C., 1992. (Eds.), Advances in modern environmental toxicology. In: Mehlman, M.A. (Ed.), Chemically-Induced Alterations in Sexual and Functional Development: the Wildlife/Human Connection, Princeton, Princeton, NJ. Colburn, T., Vom Saal, F.S., Soto, A.M., 1993. Developmental eects of endocrine-disrupting chemicals in wildlife and humans. Environ. Health Perspectives 101, 378±384. Curson, J., Quinn, D., Beadle, D., 1994. Warblers of the Americas: An Identi®cation Guide. Houghton Miin, Boston, MA.
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Patterns of organochlorine pesticide contamination in Neotropical migrant passerines in relation to diet and winter habitat J.A. Klemens
a,1
, R.G. Harper a, J.A. Frick b,*, A.P. Capparella c, H.B. Richardson a, M.J. Coey d
a Department of Biology, Illinois Wesleyan University, Bloomington, IL 61702-2900, USA Department of Chemistry, Illinois Wesleyan University, P.O. Box 2900, Bloomington, IL 61702-2900, USA c Ecology Group, Department of Biological Sciences, Illinois State University, Normal, IL 61790-4120, USA U.S. Fish and Wildlife Service, Rock Island Field Oce, 4469 48th Avenue Court, Rock Island, IL 61201-9213, USA b
d
Received 19 February 1999; accepted 19 July 1999
Abstract Eleven species of Neotropical migrant passerines collected in Illinois (USA) during May 1996, were analyzed for the presence of organochlorine (OC) pesticides. At least one of ®ve OC pesticide residues was detected in 66 of 72 birds, representing all species examined. The contaminants most frequently detected were p; p0 -DDE, dieldrin and heptachlor epoxide, all of which were present in the 10±30 ng/g range. Insectivores had signi®cantly higher levels of these compounds than did non-insectivores, while there was no signi®cant main eect of winter habitat (forest and scrub). Future research on OC pesticide contamination in resident New World passerines may allow more accurate predictions regarding the sources of contamination in Neotropical migrants. Ó 2000 Elsevier Science Ltd. All rights reserved. Keywords: Organochlorine; Neotropical migrant; Passerine; Pesticide; Diet; Winter habitat
1. Introduction Migratory birds can accumulate pesticides over vast geographic areas (Gard et al., 1995). Over the past decade there has been much interest in pesticide contamination in Neotropical migrant passerines (songbirds that winter in the Caribbean, Mexico and Central and South America, but breed in the United States and Canada). Some Neotropical migrant passerines are believed to be
* Corresponding author. Tel.: +1-309-556-3159; fax: +1-309556-3864. E-mail address: [email protected] (J.A. Frick). 1 Present address: Department of Biology, Leidy Labs, University of Pennsylvania, Philadelphia, PA 19104-6018, USA.
in decline (Robinson, 1997), and organochlorine (OC) pesticide contamination has been suggested as a possible cause for these declines (Gard et al., 1993, 1995; Block et al., 1995). However, there is a paucity of data on the extent to which Neotropical migrant passerines are exposed to such pesticides (Harper et al., 1996). The collection of baseline data is an appropriate ®rst step in evaluating the eects of pesticides on the population dynamics of Neotropical migrants (Gard et al., 1993). The purpose of this study was to document OC pesticide contamination levels in species of Neotropical migrant passerines for which few baseline data exist, and to look for patterns of contamination in relation to diet and winter habitat preferences. Analysis of diet in relation to OC contamination levels is important because insectivores may be at greater risk than non-insectivores to accumulate substantial pesticide burdens (Gard et al.,
0045-6535/00/$ - see front matter Ó 2000 Elsevier Science Ltd. All rights reserved. PII: S 0 0 4 5 - 6 5 3 5 ( 9 9 ) 0 0 5 6 1 - 5
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J.A. Klemens et al. / Chemosphere 41 (2000) 1107±1113
1995), because they are at a higher trophic level. Annually, many species of Neotropical migrants spend the greatest amount of time on their Latin American wintering grounds compared to the time spent on their breeding grounds and during migration (Keast, 1980). OC pesticides continue to be used in parts of Central and South America (Rapaport et al., 1985; Standley and Sweeney, 1995; Mora, 1997). Winter habitat preferences of Neotropical migrant passerines may indicate the relative proximity of the birds to possible sources of contamination. For example, scrub habitat that develops after forests are cleared are sometimes close to land used for agricultural purposes in the Neotropics (Capparella, pers obs), and birds that winter in such habitat may more likely be exposed to OC pesticides. 2. Methods 2.1. Collection and preparation of birds Seventy-two Neotropical migrants were either salvaged as television tower kills (N 13) or collected in mist nets (N 59). Tower kills were collected on 16 May 1996 in Livingston County, IL, USA (40° 520 , 88° 330 ). Mist netting was conducted from 14 May 1996 to 22 May 1996 at the Keithsburg Division of the Mark Twain National Wildlife Refuge in Mercer County, IL, USA (41° 060 , 90° 570 ). The birds were put on ice or dry ice at the time of collection and were later transferred to a ÿ80°C freezer for storage until they were thawed and prepared as museum skin specimens (Frick et al., 1998). The museum skins were deposited in the Illinois State University Department of Biological Sciences bird collection. The skinning procedure resulted in the skin, feathers, distal limbs, bill, partial braincase and stomach being excluded from analysis. All other parts of the carcass were included in the analysis, although the contents of the digestive tract were rinsed with distilled water in order to prevent contamination by recently ingested materials. Care was taken to remove all visible subcutaneous fat from the skins, and this fat was included in the pesticide analysis. All birds used in this study were classed as ``After Hatch Year'' (AHY), which was based upon the US Fish and Wildlife Service Bird Banding Laboratory method of assigning all individuals collected after 1 January, but before the breeding season, as AHY. After preparing the study skin, the carcass was refrozen until chemical analyses could be performed. 2.2. Residue analysis Analyses were performed using gas chromatography (Frick et al., 1998). The chemicals assayed for were aldrin, 2,2-Bis(4-chlorophenyl)-1,1-dichloroethane
(p,p0 -DDD), 2,2-Bis(4-chlorophenyl)-1,1-dichloroethylene (p,p0 -DDE), 2,2-Bis(4-chlorophenyl)-1,1,1-trichloroethane (p,p0 -DDT), dieldrin, endosulfan I, endosulfan II, endosulfan sulfate, endrin, endrin aldehyde, heptachlor, heptachlor epoxide, alpha-hexachlorocyclohexane, beta-hexachlorocyclohexane, delta-hexachlorocyclohexane, lindane, and methoxychlor. Detection limits were 0.01 lg for all pesticides except the following: heptachlor (0.02 lg), aldrin (0.03 lg), endosulfan I (0.03 lg) and endosulfan sulfate (0.10 lg). Levels of OC pesticides in duplicate samples were within ®ve percent of each other. 2.3. Statistical analysis Only p,p0 -DDE, dieldrin, and heptachlor epoxide were found in a sucient number of carcasses for statistical analyses. All concentrations that were below detection limits were treated as zeros. Mean pesticide levels were calculated for all 11 species and were used in the following analyses because of the variable sample sizes among species (see Table 1). These means were then log transformed to meet the assumption of normality. Birds were categorized according to diet (i.e. insectivore and non-insectivore) based on their primary diet during the breeding season (Ridgely and Tudor, 1989; Payne, 1992; Rappole et al., 1993; Briskie, 1994; Curson et al., 1994; Ridgely and Tudor, 1994; DeGraaf and Rappole, 1995; Kricher, 1995; McCarty, 1996; Stotz et al., 1996; Lanyon, 1997). Winter habitat preferences (i.e. forest and scrub) were taken from previous studies (Waide, 1980; Robbins et al., 1989). Diet and winter habitat preferences were analyzed with two-way ANOVA (Sokal and Rohlf, 1995) independently for each of the three compounds listed above, using SPSS software (Norusis, 1993). One-way ANOVA (Sokal and Rohlf, 1995) was used when interaction terms were signi®cant. Data reported are untransformed means and upper 95% con®dence limits (Sokal and Rohlf, 1995). 3. Results At least one of ®ve OC pesticide residues was detected in 66 of 72 birds, representing all species examined (Table 1). In addition to the most frequently detected compounds in Table 1, ®ve birds also contained p,p0 -DDT and four birds contained p,p0 -DDD. Six individuals of four species contained OC levels below detection limits. Insectivores contained signi®cantly higher levels of p,p0 -DDE, dieldrin, and heptachlor epoxide than did non-insectivores (Tables 2 and 3). There was no significant main eect of winter habitat type on levels of p,p0 DDE, dieldrin, and heptachlor epoxide. The interaction between diet and winter habitat type was not signi®cant
b
Number contaminated. Con®dence limit. c Insectivore. d Forest winter habitat. e Scrub winter habitat. f Non-insectivore.
a
c; d
Great-crested Flycatcher (Myiarchus crinitus) Least Flycatcherc;e (Empidonax minimus) Eastern Wood Peweec;e (Contopus virens) Swainson's Thrushf ;d (Catharus ustulatus) Warbling Vireoc;d (Vireo gilvus) Black-and-white Warblerc;d (Mniotilta varia) Prothonotary Warblerc;d (Protonataria citrea) Yellow Warblerc;e (Dendroica petechia) Common Yellowthroatc;e (Geothlypis trichas) Rose-breasted Grosbeakf;e (Pheucticus ludovicianus) Indigo Buntingf;e (Passerina cyanea)
Species
6 10 3 7
6 10 5 10
11.74 + 9.31
1.36 + 2.49
251.67 + 443.00 391.43 + 791.69
4.94 + 3.46 39.40 + 26.26 20.85 + 141.67 4.57 + 3.10 53.20 + 53.66 70.94 + 36.06 4.40 + 35.28
5
3
6 8
2 5 1 6 5 7 5
NC
4 5 2 7 5 10 5
Dieldrin
NCa
x 95% CLb
p,p0 -DDE
Levels of OC contaminants (ng/g)
5 5 2 9 5 10 5
N
3.07 + 3.20
1.80 + 4.12
60.00+63.46 15.86 + 8.33
2.84 + 4.91 38.80 + 11.36 22.00 + 279.54 8.48 + 7.65 15.04 + 8.04 18.90 + 12.42 15.20 + 10.77
x 95% CL
Table 1 Means and upper 95% con®dence limits of the most frequently detected OC contaminants in Neotropical migrant passerines
1
2
4 7
2 5 1 6 3 8 5
0.17 + 0.37
0.57 + 1.28
27.17 + 29.45 14.95 + 8.79
2.28 + 3.88 25.60 + 9.23 12.50 + 158.83 4.89 + 4.24 11.60 + 14.20 12.54 + 7.08 13.58 + 6.82
x 95% CL
Heptachlor epoxide NC
J.A. Klemens et al. / Chemosphere 41 (2000) 1107±1113 1109
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J.A. Klemens et al. / Chemosphere 41 (2000) 1107±1113
Table 2 Results of two-way analysis of variance of most frequently detected OC levels in relation to diet and winter habitat type of Neotropical migrant passerines Eect
Compounda p,p0 -DDE
Diet Winter habitat type Diet ´ winter habitat type a
Dieldrin
Heptachlor epoxide
F
P
F
P
F
P
6.97 0.28 0.45
0.03 0.61 0.53
7.61 0.06 5.42
0.03 0.82 0.05
22.17 3.81 13.39
0.002 0.09 0.008
df 1; 7 for all entries.
Table 3 Mean and upper 95% con®dence limits of OC contamination levels for Neotropical migrant passerines in relation to diet and winter habitat Category
Na
Levels of OC contaminants (ng/g) Dieldrin
Diet Insectivores Non-insectivores Winter habitat Forest Scrub a b
Heptachlor epoxide b
x 95% CL
x 95% CL
8 3
23.58 + 14.87 4.45 + 8.81
15.03 + 6.69 1.87 + 6.50
5 6
12.09 + 7.94 23.59 + 23.54
8.98 + 6.28 13.49 + 12.25
The same species were categorized according to diet and winter habitat. Con®dence limit.
for p,p0 -DDE; however, it was signi®cant for dieldrin and highly signi®cant for heptachlor epoxide. For insectivores there were no signi®cant dierences in contamination levels of dieldrin in forest and scrub habitats F1;6 3:91; P 0:10, and heptachlor epoxide in forest and scrub habitats F1;6 3:21; P 0:12. However, for birds that winter in scrub habitat, insectivores had signi®cantly higher levels of dieldrin (x 34:16 65:62 ng/ g) compared to non-insectivores (x 2:43 10:46 ng/g; F1;4 29:07; P 0:006). Likewise, insectivores that winter in scrub habitat also had signi®cantly higher levels of heptachlor epoxide (x 20:05 31:84 ng/g) than did non-insectivores (x 0:37 2:92 ng/g; F1;4 75:40; P 0:001). 4. Discussion These ®ndings demonstrate that OC pesticide contamination is ubiquitous in the Neotropical migrant passerines examined in our study. These results were consistent with a recent study (Harper et al., 1996) in regard to both frequency of occurrence and level of contamination. Levels of contamination ranged across six orders of magnitude, while average levels were lower than those reported in other studies (DeWeese et al., 1986; Baril et al., 1990; Fyfe et al., 1990; Mora and Anderson, 1991). This study and another study (Harper
et al., 1996) provide a baseline level of pesticide contamination for Neotropical migrant passerines utilizing the Mississippi River ¯yway. The presence of higher levels of OC contamination in insectivores than in non-insectivores is not surprising, since insectivores occupy a higher trophic level than do non-insectivores. Similar results at these and higher levels (in the lg/g range) have been found in studies of other passerine and non-passerine species (Enderson et al., 1982; DeWeese et al., 1986; Fyfe et al., 1990). Insectivorous Neotropical migrant passerines may thus be at higher risk for possible deleterious eects from OC pesticides than non-insectivores. There was no eect of winter habitat on OC contamination levels. Neotropical scrub habitats that develop after forests are cleared are sometimes in close proximity to land used for agricultural purposes. Therefore, we predicted that scrub birds would have higher OC levels than forest birds, but this was not observed. It is possible that the birds in our sample winter in naturally occurring scrub habitat that may not be in close proximity to agricultural lands. The lack of signi®cant main eect of winter habitat and the signi®cant interaction of diet and habitat type for dieldrin and heptachlor epoxide may possibly be explained by the small sample size of non-insectivorous birds in this study (one species, Catharus ustulatus) that winter in scrub habitats.
J.A. Klemens et al. / Chemosphere 41 (2000) 1107±1113
With baseline data indicating that OC pesticide contamination is common in Neotropical migrant passerines, future research on this topic should focus on two major areas. The ®rst is determining what, if any, deleterious eects low-level OC pesticide contamination has on passerines. Organochlorine contaminants have been shown to aect avian reproduction in subtle but potentially disastrous ways (Colburn et al., 1993), but little toxicological research has explicitly focused on passerines (Gard et al., 1993). What remains to be determined is if contamination at the levels detected in this study will lead to reproductive problems in these passerines. Other studies on passerines have documented no apparent eects on reproductive success in passerines with OC compounds in the lg/g range. Elliott et al. (1994) found no reproductive eects in a population of American robins (Turdus migratorius) with eggs contaminated with p,p0 -DDE at levels of 80 lg/g. Custer et al. (1998) found that the concentration of polychlorinated biphenyls (PCBs) of up to 10 lg/g in tree swallow (Tachycineta bicolor) eggs did not seem to aect hatching success. Bishop et al. (1999) found no eect on hatching success or ¯edging rates of tree swallows contaminated with p,p0 -DDE and PCBs at levels up to 11.1 lg/g. In contrast, McCarty and Secord (1999) documented reduced nest quality, a trait correlated with lower reproductive success, in tree swallows contaminated with PCBs in the 5±25 lg/g range. However, none of these studies investigated possible multigenerational eects of these OC compounds, whose eects can also vary among species (Colborn and Clement, 1992). The second area future research should address is determining the sources of OC pesticide contamination, which may also have conservation implication for raptorial birds that feed upon passerines. Neotropical migrant passerines may acquire OC compounds on their Neotropical wintering grounds, where OC pesticides may still be widely used (Rapaport et al., 1985; Standley and Sweeney, 1995; Mora, 1997). Migrants may also acquire them in the Nearctic, where many OC pesticides have been banned, but have been historically applied in great quantities (DeWeese et al., 1986). A third possibility is that Neotropical migrants may be exposed to OC compounds on feeding stops during migration. Migrating birds often stop to rebuild fat reserves, which can result in increases in body mass of up to 10% in a single day (Moore and Kerlinger, 1990; Moore and Simons, 1992). The pesticides documented in this study may be acquired at such feeding stops and may not represent levels acquired over long periods of time. However, it should be noted that OC levels may in fact represent accumulation from more than one of these sources. Organochlorine pesticide ``hotspots'' still exist in many parts of the Nearctic and Neotropics (Simonich and Hites, 1995; Blais et al., 1998). In Mexico DDT is applied to control outbreaks of malaria (Mora, 1997),
1111
while the current usage of dieldrin and heptachlor is unknown. Comparison of OC contamination in resident passerine avifaunas throughout the new world with those levels encountered in Neotropical migrant passerines may allow more accurate predictions regarding the sources of OC contamination. Acknowledgements We thank the National Science Foundation (BIR9601523) for support to purchase the gas chromatograph, and Illinois Wesleyan University for partial support of this work through an Artistic and Scholarly Development Grant to Harper and Frick. A. Bartuszevige, V. Flanagin, N. Laurie and M. Wieland assisted with pesticide extraction, and S. Janota and F. Hollingworth assisted with collection of specimens. S. Soukup, J. Hu and two anonymous reviewers made helpful suggestions that improved the manuscript. References Baril, A., Elliott, J.E., Somers, J.D., Erickson, G., 1990. Residue levels of environmental contaminants in prey species of the peregrine falcon, Falco peregrinus, in Canada. Can. Field-Nat. 104, 273±284. Bishop, C.A., Mahony, N.A., Trudeau, S., Pettit, K.E., 1999. Reproductive success and biochemical eects in tree swallows (Tachycineta bicolor) exposed to chlorinated hydrocarbon contaminants in wetlands of the Great Lakes and St. Lawrence River basin, USA and Canada. Environ. Toxicol. Chem. 18, 263±271. Blais, J.M., Schindler, D.W., Muir, D.C.G., Kimpes, L.E., Donald, D.B., Rosenberg, B., 1998. Accumulation of persistent organochlorine compounds in mountains of western Canada. Nature 395, 585±588. Block, W.M., Finch, D.M., Brennan, L.A., 1995. Single-species versus multiple-species approaches for management. In: Martin, T.E., Finch, D.M. (Eds.), Ecology and Management of Neotropical Migratory Birds: a Synthesis and Review of Critical Issues. Oxford University Press, Oxford, pp. 461±476. Briskie, J.V., 1994. Least ¯ycatcher (Empidonax minimus). In: Poole, A., Gill, F. (Eds.), The Birds of North America, vol. 99, The Academy of Natural Sciences, Philadelphia, Pennsylvania and The American OrnithologistsÕ Union, Washington, D.C. Colborn, T., Clement, C., 1992. (Eds.), Advances in modern environmental toxicology. In: Mehlman, M.A. (Ed.), Chemically-Induced Alterations in Sexual and Functional Development: the Wildlife/Human Connection, Princeton, Princeton, NJ. Colburn, T., Vom Saal, F.S., Soto, A.M., 1993. Developmental eects of endocrine-disrupting chemicals in wildlife and humans. Environ. Health Perspectives 101, 378±384. Curson, J., Quinn, D., Beadle, D., 1994. Warblers of the Americas: An Identi®cation Guide. Houghton Miin, Boston, MA.
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