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Results and evaluation of the first study of organochlorine contaminants (PCDDs, PCDFs, PCBs and DDTs), heavy metals and metalloids in birds from Baja California, México
Environmental Pollution 133 (2005) 139–146 www.elsevier.com/locate/envpol
Results and evaluation of the first study of organochlorine contaminants (PCDDs, PCDFs, PCBs and DDTs), heavy metals and metalloids in birds from Baja California, Me´xico Begon˜a Jime´neza,*, Ricardo Rodrı´ guez-Estrellab, Rube´n Merinoa, Gema Go´meza, Laura Riverab, Marı´ a Jose´ Gonza´leza, Esteban Abadc, Josep Riverac a
Department of Instrumental Analysis and Environmental Chemistry, Institute of Organic Chemistry, CSIC, Juan de la Cierva 3, 28006 Madrid, Spain b Centro de Investigaciones Biolo´gicas del Noroeste, Mar Bermejo 195, Apdo. Postal 128, La Paz, Baja California Sur, Me´xico c Department of Ecotechnologies, Research and Development Center, CSIC, Jordi Girona, 18-26, 08034 Barcelona, Spain Received 13 October 2003; accepted 14 May 2004
‘‘Capsule’’: The first data on contaminants in birds from Baja California is given. Abstract Organochlorine compounds (OCs) including polychlorinated dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs), polychlorinated biphenyls (PCBs) and 1,1-dichloro-2,2-bis( p-chlorophenyl)ethylene ( p-p0 -DDE), heavy metals (Pb, Cd, Zn, Cu), and arsenic were measured in house sparrows (Passer domesticus) and common ground doves (Columbina passerina) from Baja California Sur, Me´xico. Concentrations of PCDD/Fs were low, with 21 pg/g for house sparrows, and 7.7 pg/g for common ground doves. Nonortho-PCB concentrations in house sparrow and common ground doves were 58 and 254 pg/g, respectively, and are within the highest concentrations reported in species that are in the low levels of food webs. The major differences in organochlorine levels between species were found for ortho-PCBs and DDTs. ortho-PCB levels were higher in the seedeater species, whereas DDT levels were higher in the omnivorous species. Heavy metal levels were far below those associated with negative effects. Ó 2004 Elsevier Ltd. All rights reserved. Keywords: PCDDs; PCDFs; PCBs; DDTs; Heavy metals; Common ground dove; House sparrow; Me´xico
1. Introduction In the last five decades, many wildlife populations all over the world have experienced severe declines. Among the probable causes of decline, the negative effects of chemicals have received particular attention for research (Cade et al., 1988; Falkenberg et al., 1994; Mora, 1996). * Corresponding author: Tel.: C34 91 5622900x236; fax: C34 91 5644853. E-mail address: [email protected] (B. Jime´nez). 0269-7491/$ - see front matter Ó 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2004.05.014
It is well known that some chemicals, in particular organochlorines, interfere with the functioning of reproductive, endocrine, immune and nervous systems (Yamashita et al., 1993; Jime´nez, 1997). It has been widely reported that the decline of bird populations is associated with an increase in the use of pesticides for insect control in urban and agricultural environments (Cade et al., 1971; Peakall, 1974; Colborn, 1995). Persistent pesticides with known or suspected estrogenic and antiandrogenic activity, such as DDT and its metabolites, were used heavily on vegetable crops in
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Baja California Sur (Me´xico) before their use was banned in the 1970s–1980s (Mora et al., 1987; Wainwright et al., 2001). Several authors have suggested that birds could be used for monitoring pollution levels in terrestrial environments (Furness et al., 1993). Many of these studies have been carried out using top predators as sentinel species. Species with small home ranges are more useful bioindicators when studies at the local scales are done. There are actually quite a few studies of OC contaminants and heavy metal pollution in passerines (Bishop et al., 1995; Eens et al., 1999; Dauwe et al., 2003). In their study Dauwe et al. (2003) illustrated that passerines with a limited home range are suitable biomonitors for terrestrial organochlorine and heavy metal contamination and adequately reflect the contamination of the local environment. In 2000, we initiated studies on the effects of chemicals on birds at Baja California Sur, Me´xico. The studies initially considered a broad array of inorganic and organic chemicals that were known or suspected to occur in the area. The current status of contaminant residues (organochlorines and heavy metals) in house sparrows (Passer domesticus) and common ground doves (Columbina passerina) in Baja California Sur is examined. Although persistent pesticides have decreased in use since the last 20–30 years because they have been officially prohibited, we suspected that they are still being used for spraying crop fields. Additionally, the industrial activity in Baja California Sur is very localized and scarce, mostly concentrated in the southernmost part near La Paz town. This study presents the first evaluation of the current status of organochlorine contaminants, heavy metals and metalloids in birds from Baja California Sur using two species with different diet habits.
2. Materials and methods 2.1. Sampling sites and bird survey The study sites were located primarily in southern Baja California, Me´xico. During June–September 2000 and February–September 2001, we used a net-trapping method to catch birds. Six equal sized mist nets were placed at the edge of crop fields, inside them and near water sources. We selected two bird species, the common ground dove and the house sparrow, to evaluate the levels of organochlorine compounds, including PCDDs, PCDFs, PCBs and DDTs, and the potential effects on birds associated to crop fields in Baja California Sur. Both species were common in the study area and have been recorded foraging at crop fields and small ranches established inside the cultivated areas. Common ground doves are seedeaters, while house
sparrows are omnivorous birds. Twenty-five house sparrows and 25 common ground doves were collected under appropriate federal and institutional permits. Once the birds were collected, specimens were euthanized and liver and fat content was removed and stored at 35 C until analysis. 2.2. Residue analysis Liver was used for residue analysis. Since the amount available for each individual sample was extremely low for residue analysis, it was found more convenient to use pooled samples in our study. Pooled samples were prepared for each species to be studied, consisting of 25 individuals per species, so two pooled samples were analyzed. Turle and Collins (1992) have shown that there are no significant differences between mean residue levels determined using individual and pooled samples. The procedure of pooling samples for chemical analysis has been successfully used in many studies concerning long term monitoring programs (Bishop et al., 1992). Analyses of copper (Cu), zinc (Zn), lead (Pb), cadmium (Cd) and arsenic (As) were carried out by atomic absorption spectrometry using a calibration regression line for each element, applying the standard addition method or external standard depending on the identity and the expected concentration of each element. For the instrumental determination, a portion of the sample was digested using an acid medium following a methodology previously published (Herna´ndez et al., 1999). Analyses of Zn were performed using a flame atomic absorption spectrometer (AAS) (Spectra A-100, Varian Ibe´rica, Spain). Cd, Pb and As were measured using a Perkin–Elmer longitudinal AC Zeeman (AAnalyst 600) AAS equipped with a transversely heated graphite atomizer (Perkin–Elmer Hispania, S.A., Madrid, Spain). Copper was measured with either instrument depending on the expected concentration in the samples studied. All specimens were analyzed in batches, with method blanks, known standards, and reference material. Accepted recoveries of reference material ranged from 88 to 110%. Relative standard deviation in replicates and reference material was always below 10%. The following organochlorine compounds were analyzed: all the 2,3,7,8-substituted PCDDs and PCDFs; PCB congeners including ortho-PCBs (# 28, 52, 95, 101, 123, 149, 118, 114, 153, 132, 105, 138, 167, 156, 157, 180, 170, 189, 194) and non-ortho-PCBs (# 77, 126, 169); and DDTs (DDT and its metabolites, TDE and DDE). Sample treatment involved three steps as described previously by Bordajandi et al. (2001). First, the extraction step was carried out using a solid phase matrix dispersion procedure, which basically consisted of lowpressure chromatography on neutral and base-modified silica gel. Approximately 3 g of fresh tissue were used for
B. Jime´nez et al. / Environmental Pollution 133 (2005) 139–146
residue analysis. All samples were ground in a mortar with anhydrous sodium sulphate and were extracted with an acetone:hexane mixture (1:1 v/v). Further clean up and lipid removal was achieved by using acid- and basemodified silica gel multilayer columns. The lipid content was determined gravimetrically. The final fractionation step was achieved using SupelcleanÔ Supelco ENVIÔCarb tubes as described elsewhere (Molina et al., 2000). Three fractions were collected: the first fraction contained the bulk of PCBs and DDTs; the second and third fractions contained non-ortho-substituted PCBs and PCDD/Fs, respectively. Separation and quantification of ortho-PCBs and DDTs were carried using a Hewlett–Packard 6890 HRGC equipped with a 63Ni m-electron capture detector. A DB-5 fused silica capillary column (60 m ! 250 mm and 0.25 mm film thickness) was used. The carrier gas was nitrogen at a head pressure of 192.2 kPa. Detector and injector temperatures were 300 and 270 C, respectively. Separation and quantification of PCDDs, PCDFs and non-ortho-PCBs were performed by HRGC–HRMS on a GC 8000 series gas chromatograph (Carlo Erba Instruments, Milan, Italy) equipped with a CTC A200S autosampler and coupled to an AutoSpec Ultima mass spectrometer (Micromass, Manchester, UK), using a positive electron ionization (EIC) source and operating in the SIM mode at 10,000 resolving power (10% valley definition). The current trap was 600 mA, the ionization energy was 31 eV and the acceleration voltage was 8000 V. Ion source temperature was 250 C. The two most abundant ions in the [M Cl]C cluster ions were monitored between 50 and 80 ms dwell time and a delay time of 20 ms as described in USEPA method 1613. Chromatographic separation was achieved with a DB-5 (J&W Scientific, CA, USA) fused silica capillary column (60 m ! 0.25 mm ID, 0.25 mm film thickness) with helium as carrier gas in the splitless injection mode (1–2 mL). Chromatographic windows for each group of PCDD/PCDF homologues, from tetra- to octachlorinated, were defined on the DB-5 capillary column. Injector temperature was 280 C for the DB-5 column. The interface temperature was 280 C. The temperature program was: 140 C (1 min) to 200 C (1 min) at 20 C/min, then at 3 C/min to 300 C and held isothermally for 20 min at 300 C (Abad et al., 1997). Quantification was carried out by the isotopic dilution method (USEPA 1613, 1994). Quality assurance criteria were based on the applications of the quality control (QC) and quality assurance (QA) measures as described elsewhere (Abad et al., 2000). 2,3,7,8-TCDD equivalents (TEQs) were estimated for PCDD/F congeners and dioxin-like PCBs with an assigned TEF value, based on the bird toxic equivalency factors (TEFs) reported in 1998 by the World Health Organization (Van den Berg et al., 1998).
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3. Results 3.1. Total PCDDs, PCDFs, and PCBs Organochlorine concentrations, including PCBs, PCDDs, PCDFs, are reported in Table 1 and are expressed on a wet weight basis (WW). Total PCDD/F concentrations in both species studied were low. House sparrows (21 pg/g WW) contained the highest concentration while common ground doves contained a total PCCD/F concentration of 7.7 pg/g (WW). In house sparrows, dioxin levels were four-fold higher than furan levels and in doves PCDD and PCDF concentrations were similar. The relative contribution from each dioxin and furan congener to the total PCDD/F levels is shown in Fig. 1. In both species, OCDD was the most abundant congener. Total levels of co-planar PCBs (# 77, 126 and 169) found in common ground doves were of 254 pg/g (WW), PCB #77 being the most abundant congener followed by PCB #126 and PCB #169. In the case of house sparrows, total co-planar PCB concentration was 58 pg/g (WW), with concentration profiles similar to those of common ground doves. Total levels of the ortho-PCBs analyzed (# 28, 52, 95, 101, 123, 149, 118, 114, 153, 132, 105, 138, 183, 167, 156, 157, 180, 170, 189 and 194) were 249 ng/g (WW) in common ground doves, while in house sparrows they were 45 ng/g, five-fold lower. The relative concentrations of the individual PCB congeners analyzed in this study are plotted in Fig. 2. It appears that for ortho-PCBs, the lower chlorinated congeners #52, #95 and #101 are the most abundant in sparrows and doves.
3.2. Calculated TEQs for PCDDs, PCDFs and PCBs Total TEQs where higher in common ground doves than in house sparrows, with a value of 15 pg/g (WW) and 5.8 pg/g (WW), respectively. In both bird species, the largest percentage contribution to total toxicity came from non-ortho-PCBs, with a percentage contribution of 54% in house sparrows and 89% in common ground doves. Regarding mono-ortho-PCBs, their contribution to total TEQs was lower than 1% in both species.
3.3. DDT, DDE and TDE DDT and its main metabolites (TDE and DDE) were found in both bird species. Levels in common ground doves were not high (34 ng/g for DDE and 1.4 ng/g for DDT). However, levels were noticeable for house sparrows, which exhibited levels of DDT of 0.5 ng/g, but DDE levels were 3669 ng/g (WW).
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Table 1 DDT, PCB, PCDD and PCDF levels and calculated TEQs in house sparrows (Passer domesticus) and common ground doves (Columbina passerina) expressed on a wet weight basis (N.Q., not quantifiable)
Congener
P. domesticus TEQ
C. passerina TEQ
ng/g
ng/g
DDE TDE DDT PCB #28 PCB #52 PCB #95 PCB #101 PCB #123 C 149 PCB #118 PCB #114 PCB #153 PCB #132 C 105 PCB #138 PCB #183 PCB #167 PCB #156 PCB #157 PCB #180 PCB #170 PCB #189 PCB #194
3669 0.3 0.5 1.2 7 5 7 4.2 2.5 0.2 6 2.5 6.1 0.5 0.3 0.2 0.1 2.2 0.9 N.Q. 0.1
Total ortho-PCBs
45
Congener 2,3,7,8-TCDF 1,2,3,7,8-PeCDF 2,3,4,7,8-PeCDF 1,2,3,4,7,8-HxCDF 1,2,3,6,7,8-HxCDF 2,3,4,6,7,8-HxCDF 1,2,3,7,8,9-HxCDF 1,2,3,4,6,7,8-HpCDF 1,2,3,4,7,8,9-HpCDF OCDF
ng/g
4.2E05 2.5E05 1.5E05 2.5E04
3E06 2.3E05 8E06
34 0.9 1.4 7.5 41 48 51 19 10 0.6 24 10 20 2.4 0.4 1.3 0.4 8.5 3.1 0.1 0.3
weight basis, WW). Cu, Cd and As levels were higher in ground doves than in house sparrows, while Pb levels were higher in house sparrows. No differences were found in Zn levels between species.
ng/g
4. Discussion
1.9E04 1E04 6.4E05 1E03
4.1E06 1.3E04 3.5E05
9E07
249
pg/g
pg/g
pg/g
pg/g
0.4 0.3 0.8 0.5 0.5 0.3 0.2 0.8 0.3 0.6
0.4 0 0.8 0.1 0.1 0 0 0 0 0
0.7 0.3 0.5 0.3 0.3 0.2 0.1 0.4 0.2 0.3
0.7 0 0.5 0 0 0 0 0 0 0
Total PCDFs
4.7
1.4
3.3
1.3
2,3,7,8-TCDD 1,2,3,7,8-PeCDD 1,2,3,4,7,8-HxCDD 1,2,3,6,7,8-HxCDD 1,2,3,7,8,9-HxCDD 1,2,3,4,6,7,8-HpCDD OCDD
0.1 1.0 1.3 2.4 0.7 4.7 5.8
0.1 1 0.1 0 0.1 0 0
0.1 0.3 0.2 0.2 0.2 0.9 2.5
0.1 0.3 0 0 0 0 0
Total PCDDs Total PCCD/Fs
16 21
1.3 2.7
4.4 7.7
0.4 1.7
PCB #77 PCB #126 PCB #169
52 5 1
2.6 0.5 0
237 15.4 1.4
11.8 1.5 0
Total co-planar PCBs 58 Total TEQs
3.1 5.8
254
13 15
3.4. Heavy metals and arsenic The levels of copper, lead, cadmium, zinc and arsenic found in the liver of the common ground dove and house sparrow are shown in Table 2 (expressed on a wet
The preliminary results obtained in birds from Baja California Sur indicate that industrial inputs of PCDDs and PCDFs in the study area do not seem to be high. The difference in profile between species shown in Fig. 1 could suggest some useful information. However, it is difficult to ascertain if the difference in relative PCDD/F concentration is associated to different exposure sources, metabolism or both of them. The high prevalence of OCDD and HpCDD in both species could be indicative of a pentachlorophenol (PCP) source (Ryan and Pilon, 1982). However, no reports were found about the presence of PCP in the study area. It is remarkable that non-ortho-PCB levels found in common ground doves are among the highest reported in birds at low trophic levels. This fact could represent a problem of concern since common ground doves are preyed upon by many predators (raptors, coyote, lynx) in the study area (Delibes et al., 1997; Rodrı´ guezEstrella and Rivera, 1997) and could be a factor influencing their health and probably their survival in case they reach toxic levels due to the biomagnification process. The prevalence of OCDD and PCB #77 in both species studied has been documented in previous studies conducted on similar species located low in the trophic web (Senthilkumar et al., 2002; Merino et al., 2002). Regarding ortho-PCB pattern (Fig. 2), low chlorinated PCBs were the most abundant as other authors previously reported in species which are low in the food web (O´lafsdo´ttir et al., 2001; Merino et al., 2002). Moving up on the food web, the higher chlorinated congeners become more abundant, with PCB #153 predominating. However, Dauwe et al. (2003) found that PCB congeners #153, #180, #138, #118 and #187 were the most abundant in fat and muscle tissue of insectivorous passerines. The pattern above described by these authors was consistent with the distribution found in great tits Parus major (Winter and Streit, 1992), mallards (Mateo et al., 1998), peregrine falcons (Jarman et al., 1993), and seabirds (Choi et al., 2001). The predominance of highly chlorinated congeners is typical for species that are high on the food web. This suggests that the composition of PCB congeners would reflect the differences of feeding habits and xenobiotic metabolizing systems among different species, as reported by Hoshi et al. (1998). In addition, it should be considered that results are very dependent on the tissue studied. Different tissues give dietary information on different
B. Jime´nez et al. / Environmental Pollution 133 (2005) 139–146 40,00
Passer domesticus
143
Columbina passerina
30,00
% 20,00 10,00
2, 3 1, ,7, 8 2, 3, -TC D 2, 7,8 3, P F 1, 4,7 eCD , 2, 3, 8-P F 4, eC 7, 1, 8- DF 2, H 3, 2, 6,7 xCD 3, , 4, 8-H F 6, 7, xCD 1, 82, F 1, 3,7 Hx C 2, , D 3, 8,9 F 4, 6, Hx 1, C 7, 2, D 8 3, -H F 4, pC 7, 8, 9- DF H pC D F O 2, C 3, D 7 1, 2, ,8-T F C 1, 3,7 D , 2, 3, 8-P D 4, e C 7, 1, 8- DD 2, H 3, x 6 C , 1, D 2, 7,8 D 1, 3,7 -Hx 2, ,8 C D 3, , 4, 9-H D 6, 7, xCD 8H D pC D D O C D D
0,00
Fig. 1. PCDDs and PCDFs pattern in house sparrows (Passer domesticus) and common ground doves (Columbina passerina).
time scales. The liver ratio of stable isotopes represents the last week’s diet, while the muscle ratio is related to the diet in the last four to six weeks (Hobson, 1993). This could explain the differences found with the studies previously reported. In the present study, the tissue analyzed was liver, which would indicate a recent contamination of the individuals. The high levels of DDE found in house sparrows suggest that DDE is still present in the study area at high concentrations. Potential sources of DDE in the study area are mostly due to a heavy use of DDT in the past. It is difficult to ascertain the effects of DDE on the populations of the species studied since no previous studies on contaminants and reproduction in wild birds nesting in the area are available. However, it is important to note that DDE level in house sparrow is much above the 1 mg/g WW described by Enderson et al. (1982) as the amount of DDE in prey of peregrine falcons to result in thin-shelled eggs and reduced reproductive success. DDE levels found in this study are within those reported in a recent study by Mora et al. (2002) in prey carcass (180–5140 ng/g WW) of peregrine falcon from Texas, USA, concluding that only rough-winged swallows, with DDE levels over 5000 ng/g WW, could be implicated in the reduced reproductive success of peregrine falcon observed in the area. The DDE levels found in house sparrows (3669 ng/g) from
Baja California Sur are close to or higher than geometric mean DDE concentrations reported by White and Krynitsky (1986) in house sparrow carcass in some areas of Texas and New Mexico. These facts reflect that DDE represents a problem of concern in Baja California Sur study area. Bartuszevige et al. (2002) reported p,p0 -DDE (ranging from 7.5 to 285.5 ng/g, carcass concentration) as the most prevalent OC compound found in grasslandnesting passerines, which is a common result in other studies with passerine birds (Bishop et al., 1995; Custer et al., 1998; Klemens et al., 2000). The study carried out by Bartuszevige et al. (2002) concluded that levels of p,p0 -DDE in birds showed a strong trophic level effect. Insectivorous birds had higher levels of contamination than omnivorous and granivorous birds. However, omnivorous birds did not have significantly higher levels of p-p0 -DDE contamination than those of granivorous birds. In our study we found DDE levels to be higher in omnivorous than in seedeater species. DeWeese et al. (1986) found that omnivorous birds had higher levels of a variety of OC compounds than the one granivorous bird they included in the study. In our study, it was found that all PCBs were higher in common ground doves, a granivorous species, compared to the omnivorous house sparrow, but DDE levels were higher in house sparrows than in common ground doves. The
30,0 25,0
Passer domesticus
Columbina passerina
%
20,0 15,0 10,0 5,0
PC
B PC 28 B PC 52 B 9 P PC CB 5 B 10 12 1 3+ 1 PC 49 B PC 118 B 11 PC PC 4 B B1 13 53 2+ 1 PC 05 B PC 138 B 1 PC 83 B PC 167 B PC 156 B 1 PC 57 B 1 PC 80 B PC 170 B PC 189 B 19 4
0,0
Fig. 2. The pattern of the concentrations (relative to ground doves from Baja California Sur, Me´xico.
P
PCB) of the individual PCB congeners analyzed in samples of house sparrows and common
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B. Jime´nez et al. / Environmental Pollution 133 (2005) 139–146
Table 2 Levels (wet weight basis) of As and heavy metals (Cu, Cd, Zn and Pb) in the two species studied
Cu (mg/g) Cd (ng/g) Zn (mg/g) Pb (ng/g) As (ng/g)
C. passerina
P. domesticus
15 387 30 91 46
5 119 25 269 25
differences in DDE concentrations between the two species studied in this work could be explained perhaps by differences in diet or foraging strategies, as reported by Mora et al. (2002). A high pattern of DDE in one species and a high pattern of PCBs in the other would suggest a different source. If we look at the DDE:PCB ratio in the two species, we can find a big difference in our study area, the value of the DDE:PCB ratio being 81 for house sparrows and 0.1 for doves. If the ratio is quite different between two species in a given area, the chances that these species are feeding on much different food sources are quite high, i.e. they are quite likely being exposed to a different suite of chemicals (Hughes et al., 1998). If sparrows feed on seeds and insects from crop fields, then they might easily be exposed to DDT that was sprayed on crops. With the doves, it would seem unlikely that seeds would be contaminated with PCBs, maybe the sand and gravel they take as grit (little stones to help digest food in the gizzard) are from a contaminated industrial site (Luttik and de Snoo, 2004). Heavy metals and As were found at low levels. Nonessential metals (Cd, Pb) as well as As levels were well below the levels considered toxic (Locke and Thomas, 1996; Scheuhammer, 1987; Camardese et al., 1990). Similar results were found for essential metals analyzed (Zn, Cu) which were lower than the levels considered to be toxic (Eisler, 1993). Heavy metal contamination in Baja California Sur study area does not seem to be a problem at the present time. Differences found in contaminant levels between both species could also be explained because these birds may have different metabolism, or different microhabitat and feeding habits, house sparrows being omnivorous and common ground doves, granivorous. It is remarkable that DDE concentration found in P. domesticus suggests the need for monitoring this compound, including more species of different trophic levels. The results presented here confirm the initial suspecion of this study and suggest the importance of further monitoring of organochlorines in Baja California Sur, including a variety of species. The use of house sparrows and common ground doves verified that substances with high stability and bioaccumulative properties, especially DDE, are present in the study area probably due to a heavy use of DDT in the past.
Nevertheless, this study detected the difficulties found in selecting a good bioindicator organism. These two species were chosen since they belong to different ecological niches, and are the most abundant in the study area. P. domesticus exhibited higher concentrations of DDE than C. passerina, while C. passerina had higher PCB concentrations; thus, both species could be classified as good biomonitors for the study region depending on the contaminant. This could be an inconclusive decision due to the small number of species studied. However, based on the present study the house sparrow seems to be the most suitable biomonitor for organochlorines of concern, such as DDT or DDE, in Baja California Sur, Me´xico. More studies are needed to determine the degree to which pesticides are affecting the trophic webs in agricultural areas of Baja California because both bird species, but mainly the common ground dove, are preyed upon by many predators in the study area.
Acknowledgements Project CSIC-CONACyT 2000-2-081 supported this study. CIBNOR provided financial support. Financial support for this research was provided by the project 186/RN-38 Consejerı´ a de Agricultura y Medio Ambiente de la Junta de Comunidades de Castilla-La Mancha. Support was also obtained from CONACyT (SEMARNAT-2002-C01-0317). Rube´n Merino received a Ph.D. fellowship from the Regional Government of Madrid (Consejerı´ a de Educacio´n y Cultura). Laura Rivera received a Ph.D. fellowship from Consejo Nacional de Ciencia y Tecnologı´ a (CONACYT, Me´xico). The authors are very grateful to two anonymous referees and Dr. Weseloh for their fruitful comments on the manuscript.
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Results and evaluation of the first study of organochlorine contaminants (PCDDs, PCDFs, PCBs and DDTs), heavy metals and metalloids in birds from Baja California, Me´xico Begon˜a Jime´neza,*, Ricardo Rodrı´ guez-Estrellab, Rube´n Merinoa, Gema Go´meza, Laura Riverab, Marı´ a Jose´ Gonza´leza, Esteban Abadc, Josep Riverac a
Department of Instrumental Analysis and Environmental Chemistry, Institute of Organic Chemistry, CSIC, Juan de la Cierva 3, 28006 Madrid, Spain b Centro de Investigaciones Biolo´gicas del Noroeste, Mar Bermejo 195, Apdo. Postal 128, La Paz, Baja California Sur, Me´xico c Department of Ecotechnologies, Research and Development Center, CSIC, Jordi Girona, 18-26, 08034 Barcelona, Spain Received 13 October 2003; accepted 14 May 2004
‘‘Capsule’’: The first data on contaminants in birds from Baja California is given. Abstract Organochlorine compounds (OCs) including polychlorinated dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs), polychlorinated biphenyls (PCBs) and 1,1-dichloro-2,2-bis( p-chlorophenyl)ethylene ( p-p0 -DDE), heavy metals (Pb, Cd, Zn, Cu), and arsenic were measured in house sparrows (Passer domesticus) and common ground doves (Columbina passerina) from Baja California Sur, Me´xico. Concentrations of PCDD/Fs were low, with 21 pg/g for house sparrows, and 7.7 pg/g for common ground doves. Nonortho-PCB concentrations in house sparrow and common ground doves were 58 and 254 pg/g, respectively, and are within the highest concentrations reported in species that are in the low levels of food webs. The major differences in organochlorine levels between species were found for ortho-PCBs and DDTs. ortho-PCB levels were higher in the seedeater species, whereas DDT levels were higher in the omnivorous species. Heavy metal levels were far below those associated with negative effects. Ó 2004 Elsevier Ltd. All rights reserved. Keywords: PCDDs; PCDFs; PCBs; DDTs; Heavy metals; Common ground dove; House sparrow; Me´xico
1. Introduction In the last five decades, many wildlife populations all over the world have experienced severe declines. Among the probable causes of decline, the negative effects of chemicals have received particular attention for research (Cade et al., 1988; Falkenberg et al., 1994; Mora, 1996). * Corresponding author: Tel.: C34 91 5622900x236; fax: C34 91 5644853. E-mail address: [email protected] (B. Jime´nez). 0269-7491/$ - see front matter Ó 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2004.05.014
It is well known that some chemicals, in particular organochlorines, interfere with the functioning of reproductive, endocrine, immune and nervous systems (Yamashita et al., 1993; Jime´nez, 1997). It has been widely reported that the decline of bird populations is associated with an increase in the use of pesticides for insect control in urban and agricultural environments (Cade et al., 1971; Peakall, 1974; Colborn, 1995). Persistent pesticides with known or suspected estrogenic and antiandrogenic activity, such as DDT and its metabolites, were used heavily on vegetable crops in
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Baja California Sur (Me´xico) before their use was banned in the 1970s–1980s (Mora et al., 1987; Wainwright et al., 2001). Several authors have suggested that birds could be used for monitoring pollution levels in terrestrial environments (Furness et al., 1993). Many of these studies have been carried out using top predators as sentinel species. Species with small home ranges are more useful bioindicators when studies at the local scales are done. There are actually quite a few studies of OC contaminants and heavy metal pollution in passerines (Bishop et al., 1995; Eens et al., 1999; Dauwe et al., 2003). In their study Dauwe et al. (2003) illustrated that passerines with a limited home range are suitable biomonitors for terrestrial organochlorine and heavy metal contamination and adequately reflect the contamination of the local environment. In 2000, we initiated studies on the effects of chemicals on birds at Baja California Sur, Me´xico. The studies initially considered a broad array of inorganic and organic chemicals that were known or suspected to occur in the area. The current status of contaminant residues (organochlorines and heavy metals) in house sparrows (Passer domesticus) and common ground doves (Columbina passerina) in Baja California Sur is examined. Although persistent pesticides have decreased in use since the last 20–30 years because they have been officially prohibited, we suspected that they are still being used for spraying crop fields. Additionally, the industrial activity in Baja California Sur is very localized and scarce, mostly concentrated in the southernmost part near La Paz town. This study presents the first evaluation of the current status of organochlorine contaminants, heavy metals and metalloids in birds from Baja California Sur using two species with different diet habits.
2. Materials and methods 2.1. Sampling sites and bird survey The study sites were located primarily in southern Baja California, Me´xico. During June–September 2000 and February–September 2001, we used a net-trapping method to catch birds. Six equal sized mist nets were placed at the edge of crop fields, inside them and near water sources. We selected two bird species, the common ground dove and the house sparrow, to evaluate the levels of organochlorine compounds, including PCDDs, PCDFs, PCBs and DDTs, and the potential effects on birds associated to crop fields in Baja California Sur. Both species were common in the study area and have been recorded foraging at crop fields and small ranches established inside the cultivated areas. Common ground doves are seedeaters, while house
sparrows are omnivorous birds. Twenty-five house sparrows and 25 common ground doves were collected under appropriate federal and institutional permits. Once the birds were collected, specimens were euthanized and liver and fat content was removed and stored at 35 C until analysis. 2.2. Residue analysis Liver was used for residue analysis. Since the amount available for each individual sample was extremely low for residue analysis, it was found more convenient to use pooled samples in our study. Pooled samples were prepared for each species to be studied, consisting of 25 individuals per species, so two pooled samples were analyzed. Turle and Collins (1992) have shown that there are no significant differences between mean residue levels determined using individual and pooled samples. The procedure of pooling samples for chemical analysis has been successfully used in many studies concerning long term monitoring programs (Bishop et al., 1992). Analyses of copper (Cu), zinc (Zn), lead (Pb), cadmium (Cd) and arsenic (As) were carried out by atomic absorption spectrometry using a calibration regression line for each element, applying the standard addition method or external standard depending on the identity and the expected concentration of each element. For the instrumental determination, a portion of the sample was digested using an acid medium following a methodology previously published (Herna´ndez et al., 1999). Analyses of Zn were performed using a flame atomic absorption spectrometer (AAS) (Spectra A-100, Varian Ibe´rica, Spain). Cd, Pb and As were measured using a Perkin–Elmer longitudinal AC Zeeman (AAnalyst 600) AAS equipped with a transversely heated graphite atomizer (Perkin–Elmer Hispania, S.A., Madrid, Spain). Copper was measured with either instrument depending on the expected concentration in the samples studied. All specimens were analyzed in batches, with method blanks, known standards, and reference material. Accepted recoveries of reference material ranged from 88 to 110%. Relative standard deviation in replicates and reference material was always below 10%. The following organochlorine compounds were analyzed: all the 2,3,7,8-substituted PCDDs and PCDFs; PCB congeners including ortho-PCBs (# 28, 52, 95, 101, 123, 149, 118, 114, 153, 132, 105, 138, 167, 156, 157, 180, 170, 189, 194) and non-ortho-PCBs (# 77, 126, 169); and DDTs (DDT and its metabolites, TDE and DDE). Sample treatment involved three steps as described previously by Bordajandi et al. (2001). First, the extraction step was carried out using a solid phase matrix dispersion procedure, which basically consisted of lowpressure chromatography on neutral and base-modified silica gel. Approximately 3 g of fresh tissue were used for
B. Jime´nez et al. / Environmental Pollution 133 (2005) 139–146
residue analysis. All samples were ground in a mortar with anhydrous sodium sulphate and were extracted with an acetone:hexane mixture (1:1 v/v). Further clean up and lipid removal was achieved by using acid- and basemodified silica gel multilayer columns. The lipid content was determined gravimetrically. The final fractionation step was achieved using SupelcleanÔ Supelco ENVIÔCarb tubes as described elsewhere (Molina et al., 2000). Three fractions were collected: the first fraction contained the bulk of PCBs and DDTs; the second and third fractions contained non-ortho-substituted PCBs and PCDD/Fs, respectively. Separation and quantification of ortho-PCBs and DDTs were carried using a Hewlett–Packard 6890 HRGC equipped with a 63Ni m-electron capture detector. A DB-5 fused silica capillary column (60 m ! 250 mm and 0.25 mm film thickness) was used. The carrier gas was nitrogen at a head pressure of 192.2 kPa. Detector and injector temperatures were 300 and 270 C, respectively. Separation and quantification of PCDDs, PCDFs and non-ortho-PCBs were performed by HRGC–HRMS on a GC 8000 series gas chromatograph (Carlo Erba Instruments, Milan, Italy) equipped with a CTC A200S autosampler and coupled to an AutoSpec Ultima mass spectrometer (Micromass, Manchester, UK), using a positive electron ionization (EIC) source and operating in the SIM mode at 10,000 resolving power (10% valley definition). The current trap was 600 mA, the ionization energy was 31 eV and the acceleration voltage was 8000 V. Ion source temperature was 250 C. The two most abundant ions in the [M Cl]C cluster ions were monitored between 50 and 80 ms dwell time and a delay time of 20 ms as described in USEPA method 1613. Chromatographic separation was achieved with a DB-5 (J&W Scientific, CA, USA) fused silica capillary column (60 m ! 0.25 mm ID, 0.25 mm film thickness) with helium as carrier gas in the splitless injection mode (1–2 mL). Chromatographic windows for each group of PCDD/PCDF homologues, from tetra- to octachlorinated, were defined on the DB-5 capillary column. Injector temperature was 280 C for the DB-5 column. The interface temperature was 280 C. The temperature program was: 140 C (1 min) to 200 C (1 min) at 20 C/min, then at 3 C/min to 300 C and held isothermally for 20 min at 300 C (Abad et al., 1997). Quantification was carried out by the isotopic dilution method (USEPA 1613, 1994). Quality assurance criteria were based on the applications of the quality control (QC) and quality assurance (QA) measures as described elsewhere (Abad et al., 2000). 2,3,7,8-TCDD equivalents (TEQs) were estimated for PCDD/F congeners and dioxin-like PCBs with an assigned TEF value, based on the bird toxic equivalency factors (TEFs) reported in 1998 by the World Health Organization (Van den Berg et al., 1998).
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3. Results 3.1. Total PCDDs, PCDFs, and PCBs Organochlorine concentrations, including PCBs, PCDDs, PCDFs, are reported in Table 1 and are expressed on a wet weight basis (WW). Total PCDD/F concentrations in both species studied were low. House sparrows (21 pg/g WW) contained the highest concentration while common ground doves contained a total PCCD/F concentration of 7.7 pg/g (WW). In house sparrows, dioxin levels were four-fold higher than furan levels and in doves PCDD and PCDF concentrations were similar. The relative contribution from each dioxin and furan congener to the total PCDD/F levels is shown in Fig. 1. In both species, OCDD was the most abundant congener. Total levels of co-planar PCBs (# 77, 126 and 169) found in common ground doves were of 254 pg/g (WW), PCB #77 being the most abundant congener followed by PCB #126 and PCB #169. In the case of house sparrows, total co-planar PCB concentration was 58 pg/g (WW), with concentration profiles similar to those of common ground doves. Total levels of the ortho-PCBs analyzed (# 28, 52, 95, 101, 123, 149, 118, 114, 153, 132, 105, 138, 183, 167, 156, 157, 180, 170, 189 and 194) were 249 ng/g (WW) in common ground doves, while in house sparrows they were 45 ng/g, five-fold lower. The relative concentrations of the individual PCB congeners analyzed in this study are plotted in Fig. 2. It appears that for ortho-PCBs, the lower chlorinated congeners #52, #95 and #101 are the most abundant in sparrows and doves.
3.2. Calculated TEQs for PCDDs, PCDFs and PCBs Total TEQs where higher in common ground doves than in house sparrows, with a value of 15 pg/g (WW) and 5.8 pg/g (WW), respectively. In both bird species, the largest percentage contribution to total toxicity came from non-ortho-PCBs, with a percentage contribution of 54% in house sparrows and 89% in common ground doves. Regarding mono-ortho-PCBs, their contribution to total TEQs was lower than 1% in both species.
3.3. DDT, DDE and TDE DDT and its main metabolites (TDE and DDE) were found in both bird species. Levels in common ground doves were not high (34 ng/g for DDE and 1.4 ng/g for DDT). However, levels were noticeable for house sparrows, which exhibited levels of DDT of 0.5 ng/g, but DDE levels were 3669 ng/g (WW).
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Table 1 DDT, PCB, PCDD and PCDF levels and calculated TEQs in house sparrows (Passer domesticus) and common ground doves (Columbina passerina) expressed on a wet weight basis (N.Q., not quantifiable)
Congener
P. domesticus TEQ
C. passerina TEQ
ng/g
ng/g
DDE TDE DDT PCB #28 PCB #52 PCB #95 PCB #101 PCB #123 C 149 PCB #118 PCB #114 PCB #153 PCB #132 C 105 PCB #138 PCB #183 PCB #167 PCB #156 PCB #157 PCB #180 PCB #170 PCB #189 PCB #194
3669 0.3 0.5 1.2 7 5 7 4.2 2.5 0.2 6 2.5 6.1 0.5 0.3 0.2 0.1 2.2 0.9 N.Q. 0.1
Total ortho-PCBs
45
Congener 2,3,7,8-TCDF 1,2,3,7,8-PeCDF 2,3,4,7,8-PeCDF 1,2,3,4,7,8-HxCDF 1,2,3,6,7,8-HxCDF 2,3,4,6,7,8-HxCDF 1,2,3,7,8,9-HxCDF 1,2,3,4,6,7,8-HpCDF 1,2,3,4,7,8,9-HpCDF OCDF
ng/g
4.2E05 2.5E05 1.5E05 2.5E04
3E06 2.3E05 8E06
34 0.9 1.4 7.5 41 48 51 19 10 0.6 24 10 20 2.4 0.4 1.3 0.4 8.5 3.1 0.1 0.3
weight basis, WW). Cu, Cd and As levels were higher in ground doves than in house sparrows, while Pb levels were higher in house sparrows. No differences were found in Zn levels between species.
ng/g
4. Discussion
1.9E04 1E04 6.4E05 1E03
4.1E06 1.3E04 3.5E05
9E07
249
pg/g
pg/g
pg/g
pg/g
0.4 0.3 0.8 0.5 0.5 0.3 0.2 0.8 0.3 0.6
0.4 0 0.8 0.1 0.1 0 0 0 0 0
0.7 0.3 0.5 0.3 0.3 0.2 0.1 0.4 0.2 0.3
0.7 0 0.5 0 0 0 0 0 0 0
Total PCDFs
4.7
1.4
3.3
1.3
2,3,7,8-TCDD 1,2,3,7,8-PeCDD 1,2,3,4,7,8-HxCDD 1,2,3,6,7,8-HxCDD 1,2,3,7,8,9-HxCDD 1,2,3,4,6,7,8-HpCDD OCDD
0.1 1.0 1.3 2.4 0.7 4.7 5.8
0.1 1 0.1 0 0.1 0 0
0.1 0.3 0.2 0.2 0.2 0.9 2.5
0.1 0.3 0 0 0 0 0
Total PCDDs Total PCCD/Fs
16 21
1.3 2.7
4.4 7.7
0.4 1.7
PCB #77 PCB #126 PCB #169
52 5 1
2.6 0.5 0
237 15.4 1.4
11.8 1.5 0
Total co-planar PCBs 58 Total TEQs
3.1 5.8
254
13 15
3.4. Heavy metals and arsenic The levels of copper, lead, cadmium, zinc and arsenic found in the liver of the common ground dove and house sparrow are shown in Table 2 (expressed on a wet
The preliminary results obtained in birds from Baja California Sur indicate that industrial inputs of PCDDs and PCDFs in the study area do not seem to be high. The difference in profile between species shown in Fig. 1 could suggest some useful information. However, it is difficult to ascertain if the difference in relative PCDD/F concentration is associated to different exposure sources, metabolism or both of them. The high prevalence of OCDD and HpCDD in both species could be indicative of a pentachlorophenol (PCP) source (Ryan and Pilon, 1982). However, no reports were found about the presence of PCP in the study area. It is remarkable that non-ortho-PCB levels found in common ground doves are among the highest reported in birds at low trophic levels. This fact could represent a problem of concern since common ground doves are preyed upon by many predators (raptors, coyote, lynx) in the study area (Delibes et al., 1997; Rodrı´ guezEstrella and Rivera, 1997) and could be a factor influencing their health and probably their survival in case they reach toxic levels due to the biomagnification process. The prevalence of OCDD and PCB #77 in both species studied has been documented in previous studies conducted on similar species located low in the trophic web (Senthilkumar et al., 2002; Merino et al., 2002). Regarding ortho-PCB pattern (Fig. 2), low chlorinated PCBs were the most abundant as other authors previously reported in species which are low in the food web (O´lafsdo´ttir et al., 2001; Merino et al., 2002). Moving up on the food web, the higher chlorinated congeners become more abundant, with PCB #153 predominating. However, Dauwe et al. (2003) found that PCB congeners #153, #180, #138, #118 and #187 were the most abundant in fat and muscle tissue of insectivorous passerines. The pattern above described by these authors was consistent with the distribution found in great tits Parus major (Winter and Streit, 1992), mallards (Mateo et al., 1998), peregrine falcons (Jarman et al., 1993), and seabirds (Choi et al., 2001). The predominance of highly chlorinated congeners is typical for species that are high on the food web. This suggests that the composition of PCB congeners would reflect the differences of feeding habits and xenobiotic metabolizing systems among different species, as reported by Hoshi et al. (1998). In addition, it should be considered that results are very dependent on the tissue studied. Different tissues give dietary information on different
B. Jime´nez et al. / Environmental Pollution 133 (2005) 139–146 40,00
Passer domesticus
143
Columbina passerina
30,00
% 20,00 10,00
2, 3 1, ,7, 8 2, 3, -TC D 2, 7,8 3, P F 1, 4,7 eCD , 2, 3, 8-P F 4, eC 7, 1, 8- DF 2, H 3, 2, 6,7 xCD 3, , 4, 8-H F 6, 7, xCD 1, 82, F 1, 3,7 Hx C 2, , D 3, 8,9 F 4, 6, Hx 1, C 7, 2, D 8 3, -H F 4, pC 7, 8, 9- DF H pC D F O 2, C 3, D 7 1, 2, ,8-T F C 1, 3,7 D , 2, 3, 8-P D 4, e C 7, 1, 8- DD 2, H 3, x 6 C , 1, D 2, 7,8 D 1, 3,7 -Hx 2, ,8 C D 3, , 4, 9-H D 6, 7, xCD 8H D pC D D O C D D
0,00
Fig. 1. PCDDs and PCDFs pattern in house sparrows (Passer domesticus) and common ground doves (Columbina passerina).
time scales. The liver ratio of stable isotopes represents the last week’s diet, while the muscle ratio is related to the diet in the last four to six weeks (Hobson, 1993). This could explain the differences found with the studies previously reported. In the present study, the tissue analyzed was liver, which would indicate a recent contamination of the individuals. The high levels of DDE found in house sparrows suggest that DDE is still present in the study area at high concentrations. Potential sources of DDE in the study area are mostly due to a heavy use of DDT in the past. It is difficult to ascertain the effects of DDE on the populations of the species studied since no previous studies on contaminants and reproduction in wild birds nesting in the area are available. However, it is important to note that DDE level in house sparrow is much above the 1 mg/g WW described by Enderson et al. (1982) as the amount of DDE in prey of peregrine falcons to result in thin-shelled eggs and reduced reproductive success. DDE levels found in this study are within those reported in a recent study by Mora et al. (2002) in prey carcass (180–5140 ng/g WW) of peregrine falcon from Texas, USA, concluding that only rough-winged swallows, with DDE levels over 5000 ng/g WW, could be implicated in the reduced reproductive success of peregrine falcon observed in the area. The DDE levels found in house sparrows (3669 ng/g) from
Baja California Sur are close to or higher than geometric mean DDE concentrations reported by White and Krynitsky (1986) in house sparrow carcass in some areas of Texas and New Mexico. These facts reflect that DDE represents a problem of concern in Baja California Sur study area. Bartuszevige et al. (2002) reported p,p0 -DDE (ranging from 7.5 to 285.5 ng/g, carcass concentration) as the most prevalent OC compound found in grasslandnesting passerines, which is a common result in other studies with passerine birds (Bishop et al., 1995; Custer et al., 1998; Klemens et al., 2000). The study carried out by Bartuszevige et al. (2002) concluded that levels of p,p0 -DDE in birds showed a strong trophic level effect. Insectivorous birds had higher levels of contamination than omnivorous and granivorous birds. However, omnivorous birds did not have significantly higher levels of p-p0 -DDE contamination than those of granivorous birds. In our study we found DDE levels to be higher in omnivorous than in seedeater species. DeWeese et al. (1986) found that omnivorous birds had higher levels of a variety of OC compounds than the one granivorous bird they included in the study. In our study, it was found that all PCBs were higher in common ground doves, a granivorous species, compared to the omnivorous house sparrow, but DDE levels were higher in house sparrows than in common ground doves. The
30,0 25,0
Passer domesticus
Columbina passerina
%
20,0 15,0 10,0 5,0
PC
B PC 28 B PC 52 B 9 P PC CB 5 B 10 12 1 3+ 1 PC 49 B PC 118 B 11 PC PC 4 B B1 13 53 2+ 1 PC 05 B PC 138 B 1 PC 83 B PC 167 B PC 156 B 1 PC 57 B 1 PC 80 B PC 170 B PC 189 B 19 4
0,0
Fig. 2. The pattern of the concentrations (relative to ground doves from Baja California Sur, Me´xico.
P
PCB) of the individual PCB congeners analyzed in samples of house sparrows and common
144
B. Jime´nez et al. / Environmental Pollution 133 (2005) 139–146
Table 2 Levels (wet weight basis) of As and heavy metals (Cu, Cd, Zn and Pb) in the two species studied
Cu (mg/g) Cd (ng/g) Zn (mg/g) Pb (ng/g) As (ng/g)
C. passerina
P. domesticus
15 387 30 91 46
5 119 25 269 25
differences in DDE concentrations between the two species studied in this work could be explained perhaps by differences in diet or foraging strategies, as reported by Mora et al. (2002). A high pattern of DDE in one species and a high pattern of PCBs in the other would suggest a different source. If we look at the DDE:PCB ratio in the two species, we can find a big difference in our study area, the value of the DDE:PCB ratio being 81 for house sparrows and 0.1 for doves. If the ratio is quite different between two species in a given area, the chances that these species are feeding on much different food sources are quite high, i.e. they are quite likely being exposed to a different suite of chemicals (Hughes et al., 1998). If sparrows feed on seeds and insects from crop fields, then they might easily be exposed to DDT that was sprayed on crops. With the doves, it would seem unlikely that seeds would be contaminated with PCBs, maybe the sand and gravel they take as grit (little stones to help digest food in the gizzard) are from a contaminated industrial site (Luttik and de Snoo, 2004). Heavy metals and As were found at low levels. Nonessential metals (Cd, Pb) as well as As levels were well below the levels considered toxic (Locke and Thomas, 1996; Scheuhammer, 1987; Camardese et al., 1990). Similar results were found for essential metals analyzed (Zn, Cu) which were lower than the levels considered to be toxic (Eisler, 1993). Heavy metal contamination in Baja California Sur study area does not seem to be a problem at the present time. Differences found in contaminant levels between both species could also be explained because these birds may have different metabolism, or different microhabitat and feeding habits, house sparrows being omnivorous and common ground doves, granivorous. It is remarkable that DDE concentration found in P. domesticus suggests the need for monitoring this compound, including more species of different trophic levels. The results presented here confirm the initial suspecion of this study and suggest the importance of further monitoring of organochlorines in Baja California Sur, including a variety of species. The use of house sparrows and common ground doves verified that substances with high stability and bioaccumulative properties, especially DDE, are present in the study area probably due to a heavy use of DDT in the past.
Nevertheless, this study detected the difficulties found in selecting a good bioindicator organism. These two species were chosen since they belong to different ecological niches, and are the most abundant in the study area. P. domesticus exhibited higher concentrations of DDE than C. passerina, while C. passerina had higher PCB concentrations; thus, both species could be classified as good biomonitors for the study region depending on the contaminant. This could be an inconclusive decision due to the small number of species studied. However, based on the present study the house sparrow seems to be the most suitable biomonitor for organochlorines of concern, such as DDT or DDE, in Baja California Sur, Me´xico. More studies are needed to determine the degree to which pesticides are affecting the trophic webs in agricultural areas of Baja California because both bird species, but mainly the common ground dove, are preyed upon by many predators in the study area.
Acknowledgements Project CSIC-CONACyT 2000-2-081 supported this study. CIBNOR provided financial support. Financial support for this research was provided by the project 186/RN-38 Consejerı´ a de Agricultura y Medio Ambiente de la Junta de Comunidades de Castilla-La Mancha. Support was also obtained from CONACyT (SEMARNAT-2002-C01-0317). Rube´n Merino received a Ph.D. fellowship from the Regional Government of Madrid (Consejerı´ a de Educacio´n y Cultura). Laura Rivera received a Ph.D. fellowship from Consejo Nacional de Ciencia y Tecnologı´ a (CONACYT, Me´xico). The authors are very grateful to two anonymous referees and Dr. Weseloh for their fruitful comments on the manuscript.
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