Environ. Sci. Techno/. 1995, 29, 604-612
Introduction
Accuind&ion of Polychlorinated Biphenyls by Nestling Tree Swall0ws, Tachycineta JOHN W. NICHOLS,*,+ CHRISTEN P . L A R S E N , I MICHAEL E . M C D O N A L D , * GERALD J . N I E M I , * A N D GERALD T. ANKLEYt
US.Environmental Protection Agency, Environmental Research Laboratory-Duluth, 6201 Congdon Boulevard, Duluth, Minnesota 55804, and Natural Resources Research Institute, University of Minnesota-Duluth, 5013 Miller Trunk Highway, Duluth, Minnesota 5581 1
A bioenergetics-based model was developed to simulate the accumulation of polychlorinated biphenyls by nestling tree swallows (Tachycineta bicolor). The model was largely parameterized using published information for passerine birds and accurately describes the observed growth of nestling swallows. The model was evaluated by comparing predicted concentrations of selected congeners with those measured in 15 d-old nestlings collected from two sites within the Saginaw River watershed. Residue concentrations in nestlings were calculated as the sum of compound inherited in the egg and that assimilated from the diet, consisting principally of emergent aquatic insects. Model predictions were in good agreement with those measured in nestlings collected from a relatively uncontaminated site but consistently overestimated concentrations in birds from an area of known sediment contamination. The cause of this discrepancy is unknown, but did not appear to be related to metabolic biotransformation of individual congeners. Instead, it is suggested that dietary composition may have varied between sites. Alternatively, food consumption by nestling birds may have been overestimated. The results of this study indicate that caution must be used when interpreting residue information from nestling swallows, which have been proposed for use as sentinels of local sediment contamination.
Concern about adverse effects of environmental contaminants on wild birds increased during the 1960s with the demonstration that DDT and related compounds in raptorial and piscivorous birds had caused widespread population declines due to eggshell thinning and resulting reproductive failure ( 1 , 2). More recently, it has been suggested that persistent polychlorinated aromatic hydrocarbons (PCHs,including polychlorinated biphenyls (PCBs), dibenzofurans (PCDFs), and dibenzo-p-dioxins (PCDDs)) have adversely affected several nonraptorial piscivorous species including Forster’s terns, common terns, blackcrowned night herons, double-crested cormorants, and herring gulls (3-9). Collectively,these studies demonstrate the potential for persistent organic compounds to biomagnlfy in aquatic food chains, culminating in a substantial dose to birds that feed at the top of these food chains. Recognition of the importance of this route of exposure has led to recent development of water-based criteria for protection of both avian and mammalian wildlife in the Great Lakes basin (10). Current interest in toxic effects on wild bird populations continues to be focused on piscivorous species. However, emergent aquatic insects may provide a second pathway by which birds can accumulate persistent environmental contaminants. Chemical residue data confirm that insectivorous birds living in or near contaminated aquatic ecosystems accumulate substantial body burdens of these compounds (11-19). In laboratory studies, chironomid larvae (Chironomus plumosus) accumulated PCBs when placed in spiked sediments, and upon emergence, PCB concentrations in adults were found to be higher than those in the larvae (20). Chironomid larvae (C. tentuns) exposed to a mixture of Aroclors accumulated each of the PCB congeners examined, but preferentially accumulated those with a low number (2-4) of chlorine substituent groups ( 2 1 ) . Larval mayflies (Hexugeniu limbutu) accumulated benzo [a]pyrene, phenanthrene, and hexachlorobiphenyl when exposed to spiked sediments (22). Mobilization of sediment-associated pollutants by emergent insects has been verified in the field (20,23-26), and spatial patterns of contamination in insects have been shown to correspond to those in sediments (27). Nevertheless, the linkage between emergent insects and contaminant levels in the animals that consume them remains largely unexplored. The purpose ofthis studywas to develop a bioenergeticsbased model for the accumulation of PCBs by nestling tree swallows (T.bicolor). The tree swallow is a widely distributed passerine bird that feeds extensively on emergent aquatic insects (28-30). Adult swallows forage within a limited area when providing for their young (28,30). These attributes have led to the suggestion that nestling swallows can be used as sentinels of local sediment contamination ( 1 9 ) . A bioenergetics-based model was employed to explicitly link chemical dose (via consumption of contaminated prey) and the mass of the bird into which the ~
* Author to whom correspondence should be addressed; Phone. (218) 720-5524. +
4
604 ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 29, NO. 3,1995
U S . Environmental Protection Agency. Natural Resources Research Institute.
0013-936X/95/0929-0604$09~00/0
B 1995 American Chemical Society
compound is diluted. These models are also amenable to incorporation of natural factors such as seasonalvariations in prey selection and abundance. Model inputs included residue concentrations in eggs and emergent insects collected during the spring and summer of 1991 from two sites located within the Saginaw River watershed (Lake Huron). Simulated residues in nestlings were evaluated by comparison with observed residue concentrations in nestlings just prior to the time of fledging.
Methods
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Bioenergetics-BasedModel. The growth of nestling tree swallows was modeled using a balanced energy equation (311,rearranged to solve for the production term:
P = C - (R+FU)
(1)
The units of each term in this equation are kcal g-l d-l. The production (P)term refers to energy invested in tissue growth and fat storage. Consumption (0is defined as the maximum rate of gross energy intake. The respiration term (R) includes energy expended for: (a) basal metabolism (BM), which is the post-absorptive metabolic rate at nonstimulatory temperatures, (b) specific dynamic action (SDA),(c) thermoregulation (TR),and (d) physical activity (A). The elimination term (FU)includes energy lost due to egestion of feces and excretion of nitrogenous waste. Growth rate (G, in g g-’ d-l) was calculated by dividing P by the caloric density of the bird (CDB). Integrating G yields the body weight of the chick (BW, in g) at each time interval. BW was used in turn to calculate C and R, both of which were expressed as allometric functions of the form: Y = aBWb, where a and p are constant values. FU was calculated as a constant fraction of C. Subtracting FU from C yields the quantity frequently referred to as “metabolizable energy” (ME). The scope of this modeling effort was limited to consideration of the “average” individual. No attempt was made to distinguish between different brood sizes. The rate of accumulation of PCBs by nestling swallows (ABB, in pg bird-’ d-l) was calculated as the product of C, BW, and PCB concentration in the insects ([PCB]), and percentage assimilation of PCBs from the diet (ASSIM), divided by the caloric density of the insects (CDI):
ABB = (C * BW [PCB] ’ ASSIM) ICDI
(2)
The total amount of chemical in the chickwas calculated by integrating ABB and adding this amount to the PCB burden inherited from the female parent (egg residue). Dividing by BW gives the concentration in the chick at each time interval. Once accumulated, PCBs were assumed to be unavailable for elimination. The model was encoded using a commercial software package (Advanced Continuous Simulation Language, Mitchell and Gauthier Assoc., Concord, MA). Differential equations were solved simultaneously by numerical integration to obtain a solution set for any time unit. Model Parameterization. The model was parameterized to the extent possible using bioenergetics information from the literature. Our intention was to create an accurate model for tree swallows,without incorporating unnecessary complexity. For example, it has been shown that for several passerine birds ME, as a proportion of C, varies during the nestling development period (32). However, these changes are relatively minor when compared to changes in allocation
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FIGURE 1. Allomatric equation for resting metabolism in nestling passerine birds. Published values are shown as individual points and ware obtained from the following species: solid circles, redbacked shrike (34); open circles, house sparrow (36);open squares yellow-eyed junco (43);solid trianglas, house sparrow (32);open The equation was f i i d to untransformed triangles,tree sparrow data by using the method of least sum of squared differences.
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of ME. We therefore elected to calculate ME as a constant proportion of C and concentrated instead on changes in the amount of energy expended for R. The energy budget of nestling tree swallowshas not been investigated; however, that of several other passerine birds has been described in considerable detail (32-43). Priority was given to information for passerine birds similar in size to swallows and which fledge within 20 d of hatching. In general, it is possible to distinguish three phases of nestling development (33, 44). The first phase is characterized by a period of rapid growth during which parents brood the young to provide heat. During the second phase, chicks begin to grow adult plumage and develop the ability to thermoregulate. The third phase is characterized by continued development of thermoregulatory ability and increased activity prior to fledgling. The net result of these changes is that R as a proportion of C increases sharply when birds begin to thermoregulate and continues to increase until fledging, albeit more slowly during the last few days in the nest. In contrast, G as a proportion of C is high during the first few days after hatching and then declines steadilythereafter. In many cases, passerine birds have been observed to lose weight during the last several days in the nest (45). Various authors have attempted to measure metabolism in passerine birds under both laboratory and field conditions. In practice, the energy costs of BM, SDA, and TR are difficult to distinguish. By convention, therefore, all three are usually combined and called “resting metabolic rate” (RMR). Published estimates of RMR were divided by BW to be consistent with units in the balanced energyequation. The data were then plotted against BW, and an allometric expression was fitted using the method of least sum of squared differences (Figure 1). The resulting values of a and p were 0.15 and 0.38, respectively. The units of this equation differ from those generally used in allometric expressions for metabolism (typicallykcal animal-’ time-’). When expressed on a whole animal basis, RMR for 47 different species of adult birds scaled to an exponent of approximately0.68(46).Thus, across speciesvaryingwidely in size, respiration increases with size less rapidly than would be predicted from a direct proportionality with weight. In nestling birds, however, increases in size of an individual animal are accompanied by proportionately larger increases in RMR. Were these data to be plotted on VOL. 29. NO. 3.1995 /ENVIRONMENTAL SCIENCE &TECHNOLOGY
605
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FIGURE 2. Allometric equation for gross energy consumption by nestling passerine birds. Published valuer are shown er idwidual points and were obtained from the following species: solid circles, open red-backed shrike (34);open circles, house sparrow squares, yellow-eyed iunco (44;solid triangles, house sparrow (32); open triangles, tree spanow (32);solid dimnoads. ash-throated open diamonds, western bluebird (8. Tbe equation flycatcher (8; was obtained by fitting model simulations to growth data from nestling tree swallows (Figure 3; see text for further details).
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FIGURE 3. Growth of nestling tree swallows from the Saginaw River watershed, Michigan, 1991. Measured values are shown as individual points; each point represents the mean of from 36 to 48 individuals. The model simulation is shown as a solid line and was fitted to untransformeddata using the method of least sum of squared differences.
a whole animal basis, the allometric exponent would be greater than 1.0. The relationship between R and BW is less well-known than that between RMR and BW because of the difficulty in obtaining measurements without affecting the activity level of the birds. Using a doubly-labeled water technique, Weathers and Sullivan (43)determined that R (referred to by the authors as FMR or "field metabolic rate") and RMR were indistinguishable in nestling juncos during the first two or three days post-hatching, after which measured values began to diverge, resulting in total energy expenditures at fledging that were approximately 1.5 times higher than resting values. We therefore calculated R as the product of RMR and an activity coefficient, the value of which was set equal to 1.0 during the first 5 days posthatching, followed by a linear increase between days 5 and 15 to a final value of 1.5. Initially, we tried to fit an allometric expression for C using the approach employed for RMR. However,literature data for Cdid not follow a consistent pattern (Figure2).We therefore developed an allometric expression for Cby fitting model predictions of growth to observed growth rates in nestlings from the Saginaw River watershed (Figure3). The body mass of nestling swallowsfollowed asigmoidal growth curve, reaching a maximum value of about 23 g on day 12 606
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 29, NO. 3, 1995
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or 13, followed by gradual weight loss until day 15 (just prior to fledging). This pattern is similar to that reported previouslyforwell-fedswallowchicks ( 47,48). When model simulations were fitted to these data, the resulting values of a and /3 were 0.64 and 0.127, respectively. Finally, we assumed that C was not limited by food availability at any time during the nestling development period. For nestling passerine birds, reported values of ME as aproportionof Cvaryfrom67.0% to 79.1%,but tend toward the lower end of this range ( 3 2 3 4 ,36, 37, 49). A value of 70% was therefore selected and was assumed to remain constant. To estimate the amount of food consumed that would be required to account for an observed rate of growth, it was necessary to correct for the caloric density of birds and insects. Developmental changes that accompany the growth of nestling birds result in an increase in CD, due to water loss and an increase in fat content (32,35,36,38,50), When these data were plotted against BW, a linear relationship was obtained, the fitted equation for which is (Figure 4)
CD = 0.037 BW
+ 0.477
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The caloric density of insects fed to nestling birds was set equal to the mean of several published values (5.4 kcal g-I dry weight; see refs 36,40, and 51-53). This value was then converted to kcal g-' wet weight by multiplying by 0.23 (mean ofvalues determined by refs 40,51, and 54) and was assumed to remain constant. The identity of prey items consumed by nestling tree swallows and the percentage of total prey items that originate from aquatic sources are likely to vary among locations and from year to year within a location. Blancher et al. (29) found that approximately half of all prey items fed to nestling swallows were of aquatic origin. Other reports suggest that the contribution of emergent insects to the diet may be higher. Dipterans (primarily chironomids) comprised approximately90% of the diet of swallows nesting near a sewage lagoon (28). St. Louis et al. (30) reported that 90% of foraging time was spent over water during egg production; however, this value declined to 57% later in the breeding cycle due to a decrease in the abundance of emerging chironomids. In the present study, birds were most frequently observed feeding over the open water of the Saginaw River or in marshes along its edge but
were also seen foraging along the river banks. We therefore parameterized the model by assuming that 70% of the nestling diet was composed of emergent insects. The balance of the diet was assumed to be made up of terrestrially-derived prey, which were further assumed to not contain PCBs. Initial Conditions. Egg weight was set equal to the average (1.6 g) of values measured at four study sites on the Saginaw River watershed. The female usually lays 1 egg/ day; however, hatching tends to be relatively synchronous (48). Therefore, the model does not distinguish between chicks of different ages. Metabolic Biotransformation. Although information on the metabolism of PCBs by birds is limited, several generalizations can be attempted. The capacity of birds to metabolize PCBs tends to vary inversely with the number of chlorine substituent groups. Compared to mammals, birds possess a reduced capacity to metabolize PCBs with higher levels of chlorine substitution (55). Moreover, metabolism of individual congeners appears to be dependent upon the presence of vicinal hydrogen atoms in the meta and para positions (meta-para-unsubstituted;5658).
It is not known whether neonatal birds possess the metabolic capabilities of adults (biotransformation pathways in mammalian neonates are ofien poorly developed or absent altogether). It is also uncertain whether the metabolism of PCBs in young birds can be induced by prior exposure of the adults (and deposition of PCBs in the egg). We therefore made the simplifyingassumption that nestling swallows do not metabolize PCBs, recognizing that if this assumption was violated the model would tend to overestimate observed residues. In this respect, underestimating metabolism has the same effect as overestimating dietary assimilation efficiency. Dietary Assimilation of PCBs. Published reports on dietary uptake of PCBs by avian wildlife are limited to a single study by Serafin (59),who used an in situ perfusion technique to study the intestinal absorption of 2,2',4,4',5,5'hexachlorobiphenyl in northern bobwhite quail (Colinus virginiunus), eastern screech owls (Otus mio), American kestrels (Fulco spurverius), black-crowned night herons (Nycticorax nycticorax), and mallard ducks (Anm platyrhynchos). Absorption rates differed markedly among the five species, leading to the suggestion that such differences could result in dissimilar uptake under normal physiological conditions. These data did not, however, provide an estimate of dietary assimilation efficiency. PCB absorption data for insectivorous birds were lacking altogether. We therefore assigned this parameter a value of 70% and then varied it to examine its effect on residue predictions. PCB Data Set. Tree swallow nest boxes were placed at four locations in the Saginaw River watershed (Figure 5 ) . The four sites were intended to represent a gradient of sediment contamination, with the most upstream site (CHIP) being the least impacted by industrial and agricultural drainage and, therefore, the least contaminated. The most downstream site, located at the mouth of the Saginaw River (COPO), was believed to be the most contaminated of the four and is within an area of known sediment contamination (60, 61). A detailed description of each study site, including the number, positioning, and occupancy rate of nest boxes, is presented elsewhere (62). Nest boxes were visited every other day from the time that egg-layingactivity began (lateApril/early May). Direct
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observations were suspended when birds reached 15 d of age to prevent premature departure from the nest (63). Eggs and nestlings were weighed to the nearest 0.1 g. Two eggs, chosen at random, were collected from nests containing at least five eggs; one egg was collected from nests having four eggs. The eggs were then composited (8- 12 eggs/sample) to provide sufficient material for chemical analysis. Two to five 15d-old nestlings were collected from each site and were analyzed individually. Eggs and nestlings were placed in solvent-rinsed glass jars immediately following their collection and frozen for later analysis. Emergent insects were collected by hand at two of the four study sites. Insects were captured with a conical net by disturbing shoreline vegetation during an observed hatch. No attempt was made to characterize the composition of these samples;however, gross examination suggested a predominance of midges (chironomidae), as would be expected of such locations during late spring and early summer. Insects were composited and weighed, providing two samples of sufficient size for analysis at one site (CHIP) qnd a single sample at a second site (COPO). The composited samples were placed in solvent-rinsed glass jars and frozen for later analysis. Analysis of the planar PCBs was based upon isotope dilution gas chromatography/high-resolution mass spectroscopy (GCIHRMS),while the nonplanar congeners were measured using gas chromatographywith electron capture detection (64, 65). Individual birds and site-specific composites of egg and insect samples were blended with sodium sulfate; spiked with 13C-labeledPCB congeners 77, 126, and 169;and extracted with hexaneIdichloromethane (1:l by volume). Solvent was removed from the samples with a Kuderna-Danish evaporator. Tissue extracts were redissolved in hexane and passed through a sulfuric acid/ celite column to remove potential interferences due to biogenic components. Planar and nonplanar PCB congeners were separated and concentrated from the samples using florid and carbon columns as described by Kuehl et al. (65) and modified by Walker et al. (66). GC/HRMS analyses were performed on a Finnigan-MAT Model 8230 in the selected ion monitoring mode, using 30-m DB-5 and DB-Diox columns for separation (64). Quantitations were based on the relative responses of analytes and the isotopically labeled internal standards measured in the samples and on relative response factors, which were VOL. 29, NO. 3, 1995 /ENVIRONMENTAL SCIENCE & TECHNOLOGY
607
TABLE 1
PCB Residues in Tree Swallow Eggs and Nestlings from Saginaw River, Michigan, 1991a sampling sitdsample type CROW eggs (2Ib nestlings (2) [% CVI AIRP eggs nestlings (2)
[% cv1 CHIP eggs (21b nestlings (3) [% CV] insects (2Ic COP0 eggs (31b nestlings (5) [% CVI insects (1)
total PCBs (ng g-1)
individual congeners (pg g-l)
homolog groups (ng g-l) penta hexa hepta octa
77
101
118
126
180
tri
tetra
nona
deca
563 171 [56.01
1707 1070 f59.11
19390 5810 L60.81
14755 5703 [54.1I
309 109 i107.31
33880 5133 L61.51
36 9
68 27
102 36
189 57
88 19
28 6
9 2
4 1
1144 616 f25.41
3073 2111 r8.41
36675 19280 L16.21
31135 18425 129.41
476 22 1 [ I 1.51
73555 25905 B.01
73 73
126 98
196 120
375 152
210 80
62 21
9 8
5 5
836 330 i26.71 90
3365 445 [24,31 34
20700 9900 [21.6] 1480
20120 8100 i31.11 1808
502 87 L18.51 ND
33550 14066 L15.91 3960
104 8
82 20
132 147
207 92
196 33
56 15
5 2
7 3
ND
45
19
14
8
2
ND
2
1373 1027 r20.91 682
4600 5850 r24.91 2666
39660 32 160 [21.6] 21110
37437 36204 f26.61 23680
685 516 i25.21 ND
64910 36298 L25.71 23900
91 90
214 202
278 212
357 245
217 117
64 41
15 9
9 4
30
148
152
144
83
28
10
10
aValues are means, sample sizes are given in parentheses. ND = not detected. % CV = (SD/mean) x 100. Each egg sample is a composite of 8-12 eggs from several nests. Data forthe two insect samples were averaged. This required that analyses which were termed "not quantifiable" be given a value, which we determined to be 10 pg g-' or approximately one-half the estimated detection limit (72).
determined from the analysis of calibration solutions containing both analytes and internal standards. Instrumental analysis of the nonplanar PCBs was performedwith a Hewlett-Packard 5890 gas chromatograph equippedwith a 60-m DB-5 capillary column and an electron capture detector. Quantitations were based on responses of analytes relative to internal standards (PCB congeners 30 and 204) added prior to chromatography. Relative retention times and response factors were determined from analyses of calibration solutions containing the internal standards and Aroclor mixtures (67). Total PCBs were calculated by summing concentrations of the individual congeners. Duplicate analyses were performed on selected samples to assess the precision of the analyticalmethod. Coefficients of variation (CV for total PCB measurements ranged from 0.8 to 6.2. Similar values were obtained for individual congeners, except when they were present at levels near the detection limit.
Results Field Observations. The spring and summer of 1991were colder and wetter than normal throughout the Saginaw River watershed. These conditions probably had a negative impact on hatching success and nestling survival among tree swallow populations at all four sampling sites (62). Nevertheless, growth rates among surviving birds were comparable to previously reported values (Figure 3; for comparison,see refs 47 and 48). An analysisof reproductive data showed that there were no significant differences among sites in clutch size, egg weight, egg volume, young hatched per nest, young fledged per nest, or maximum weight of nestlings (62). In most cases, nest departure occurred between 16 and 20 d, which is normal for tree swallows (68). PCB Data Set. PCB residues in nestlings, eggs, and insects are reported in Table 1. The data are expressed as mass of PCB per wet weight of sample to emphasize differences in concentration, irrespective of lipid content. Congener-specific data are presented for one mono-ortho(118) and two non-ortho-substituted (77 and 126)congeners 608 1 ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 29, NO. 3, 1995
as well as for PCBs 101 and 180. PCB 101 is a meta-paraunsubstituted congener that has been shown to be metabolized by adult pigeons (57) and eider ducklings (58). PCB 180 is a highly persistent contaminant of most environmental samples and is thought to be poorly if at all metabolized by birds (57). Summed values for each of the homolog groups are also presented, as is the sum of all congeners (total PCBsI for each sample type. The variation in PCB residues in chicks within sites is reported as percent coefficientof variation (% CV). These data were insufficient to permit an analysis of variance; however, the rank order of site contamination determined from sample means was consistently reflected in values for individual chicks. The rank order of total PCB concentration in both chicks and eggs by sampling site was COPO > AIRP > CHIP > CROW. Because of its location relative to the other sites, the emergence of CROW as the least contaminated site was unexpected. Unlike the other three sites, however, nest boxes at the CROW site were not located on the river itself but were instead placed within an adjacent wildlife management area (Crow Island State Game Area, see ref 62). The possibility therefore exists that residue levels in samples collected from this site do not reflect the level of contamination existing in nearby riverine sediments. At each of the sites examined, the concentration of total PCBs in eggs exceeded that in chicks. Comparing sites, the egg/ chick concentration ratio varied inversely with the degree of site contamination, declining from 3.3 at the least contaminated site (CROW) t o a value of 1.3 at the most contaminated site (COPO). Tetra-, penta-, hexa-, and heptachlorobiphenyls comprised greater than 70% of the PCBs present in both chicks and eggs. Mono- and dichlorobiphenyls were essentially absent (data not shown), while tri-, nona-, and decasubstituted congeners were present in small quantities. Without exception, the distribution of homologs in eggs peaked with the hexachlorinated congeners. This was also true of chicks at three of the four study sites. At the fourth site (CHIP), pentachlorobiphenyls were present at higher concentration than hexachlorobiphenyls.
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Nestling Age (days) FlGURE6. Energy budget predictedby the tree swallow bioenergetics model. Simulationscorrespondto model predictionsof metabolizable energy (dotted line), total respiration (solid line), and resting metabolic rata (dashed line). Energy available for productionis equal to the difference between metabolizable energy and total respiration. The difference between total respiration and resting metabolic rate is due to the energy cost of activity.
Homolog distributions dif€eredmarkedly in insects from the two sites examined, as did total PCB concentrations relative to those in eggs and chicks. At the COPO site, the homolog distribution peaked with the pentachlorinated congeners, while at the CHIP site, tetrachlorobiphenyls predominated. The total PCB concentration in insects from the COPO site was about half that in the eggs or chicks. The total PCB concentration in insects from the CHIP site was about one-tenth that in eggs and one-third that in chicks. Of the planar PCBs examined (77,81,126,118,167,169, and 1891, PCB 118 comprised the largest percentage of total PCBs in all samples. PCBs 77,81, and 167 were present at lower concentrations (10-20% that of 1181,while PCBs 126, 169, and 189 were present in very small quantities or were not detected. Other planar PCBs (particularly PCB 105) were probably present in most or all samples but could not be quantified due to coelution with other congeners. The contribution of egg residues to chemical burdens in nestlings was estimated by dividing the mass of PCBs in eggs by that in the chicks (mean weight at 15 d = 22.1 g). Insects were assumed to contribute the balance of measured residue levels. Eggs contributed from 9.7%to 23.8%oftotal PCB residues in chicks. The extent of this contribution varied inversely with the degree of site contamination due to the previously described inverse relationship between site contamination and egg/chick concentration ratio. In most cases, similar values were obtained for the individual congeners, although in several instances (e.g., PCB 180 at the CROW site and PCB 77 at the CHIP site) the egg contribution was close to that of insects. These exceptions did not, however, suggest any patterns related to congener or site. Bioenergetics Model. The model qualitatively reproduced the pattern of ME allocation observed in studies with passerine birds (Figure 6; for comparison, see refs 36 and 43). Integrating the area under each curve yielded an estimate of the total amount of energy expended for each type of docation. These estimates are in good agreement with published values, although production as a percentage of total energy consumption is slightlyless than the lowest reported figure (Table 2). Residue Predictions. Simulated PCB residues in nestling birds were obtained by using residue levels in eggs and insects collected from the CHIP and COPO sites as inputs to the model. At both sites, the model predicted that total
PCB residue concentrations in chicks would decrease rapidly during the first few days of nestling development, followed by an increase in concentration until fledgling, the extent of which was dependent upon residues in the insects. The total mass of PCBs contained in nestling birds was predicted to increase slowly during the first few days after hatching and more rapidly thereafter (Figure 7). Efforts to model individual PCB congeners gave results for each site that were qualitativelysimilar to those obtained for total PCBs. These results are reported in Table 3 as the percentage difference between observed and predicted residues in 15-dold birds. In general, the model accurately predicted chemical residues observed in chicks collected from the CHIP site despite large differences in congener concentrations in insects and the possible influence of metabolic biotransformation. In contrast, the model consistently overestimated residues measured in chicks from the COPO site. Reducing chemical assimilation efficiency or the percentage of diet derived from aquatic insects from 70% to 30% resulted in close correspondence between model predictions and observed residues. However, the same manipulations caused the model to underestimate observed residues at the CHIP site by a factor of 2 or more.
Discussion The reproductive biology of tree swallows provides an opportunity to investigate the role that emergent aquatic insects play in mobilizing sediment-associated environmental contaminants. Throughout their breeding range, tree swallow population densities are limited by the availability of suitable nesting cavities (68). Study populations can therefore be created by providing the birds with artificial nest boxes. PCBs, DDE, and several other organochlorine compounds have been measured in tree swallows from Central Alberta, the western United States, and the Great Lakes region (11-13, 19). To date, however, evidence for adverse effects due to the accumulation of these compounds has been limited to anecdotal accounts (68).
The objective of this effort was to develop a bioenergetics-based model for the accumulation of PCBs by nestling tree swallows. It was not our intention to “fit” model outputs to observed data, but instead to use the model to investigate factors that are likely to influence chemical bioaccumulation. The utility of this approach can be demonstrated by examining changes in residue concentrations after hatching. Contaminant levels in chicks were consistently lower than those in eggs, presumably due to high rates of growth, relative to the rate of chemical absorption. This outcome is frequently referred to as “growthdilution” and has been reported for young herring gulls (69),shags (Phalacrocoraxaritotelis;70),whitethroats (Sylvia communis;711, and Forster’s terns (8,15). Growth dilution was also noted recently in tree swallows by Bishop et al. (19). Closer examination of the Saginaw data set suggests that the extent of growth dilution varied within (total PCBs vs each congener, one congener vs another) and among (total vs total, one congener vs the same congener) sampling sites, and in at least one case (COPO, PCB 77) residues in chicks were higher than those in eggs. Perhaps most significantly, there appeared to be a general trend toward decreased growth dilution with increasing degree of site contamination. VOL. 29. NO. 3, 1995 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
609
TABLE 2
Observed and Predicted Cumulative Energy Balance for Passerine Birds during Nestling Development PerioP
c
species, age
consumption
z
metabolizable energy
respiration
production
Z consumption x 100
source
tree swallow, 15 d tree sparrow, 15 d house sparrow, 15 d red-backed shrike, 15 d house sparrow, 17 d ash-throated flycatcher, 17 d western bluebird, 21 d yellow-eyed junco, 12 d
224 160 200 194 290 3506 3796 1646
157 122 157 136 199 245 265 115
137 97 125 97 161 210 226 94
20 25 32 39 38 35 39 21
9 16 16 20 13 10 10 13
this studyC 32 32 34 36 42 42 43
c
c production/
*All values are reported as kcal bird-' and were obtained by integrating over the duration of the nesting development period. Calculatedfrom total metabolizable energy by assuming that energy assimilation efficiency was 70%. Predicted by the model.
60 7
- 50 0,
3
v
2
z
40
s r-"
a
9 2.5
v
C 0
.= 2.0 E c
C
m 30
k!-
....
3.0 1
v -
20
1.5
C
../
0"m
1.0
a
0.5
0
10 0
s
T
........
...........
9
CHIP
A
...................................
..........
0.0
3
0
9
6
15
12
Nestling Age (days) FIGURE 7. Simulated and observed total PCB residues in nestlings from the CHIP and COPO sites. The mean concentration (& SD) of total PCBs measured in 15 d-old nestlings is shown as an open circle (CHIP n = 3) or open square (COPO; n = 5). Model simulations are shown as solid (PCB concentration) and dashed (PCB mass) lines. Simulations were obtained by using the PCB concentrations in insects and that contained in the eggs as inputs to the model. All model parameters were set equal to values given in the text. 2.0 -1
TABLE 3
/
Observed and Predicted PCB Concentrations in Nestling Tree Swallows" CHIP obs
pred
420 total PCBs 330 PCB 77 0.44 0.38 9.90 7.40 PCB 101 PCB 118 8.10 8.66 PCB180 14.07 18.18
COP0
YO dif* +27 -14 -25 +7 +29
obs
pred
2810 1027 5.85 10.91 32.16 86.62 36.20 96.64 36.30 99.55
YO difb +I73 +86 +I69 +I67 +I74
PCBconcentrationsarereported as ng g-l. (Observed-predicted)/ observed x 100.
By simulating the results of a hypothetical exposure, it can be shown that differences in the extent of growth dilution at a given stage of development are to be expected depending on the contaminant concentration in the diet (Figure 8). This result suggests that the appearance of growth dilution at one study site and not another or only during very early stages of development in one species, while persisting for an extended period in another, may be due to varying contaminant levels in prey items and does not of itself indicate differences in chemical disposition. The overestimation of observed residues in nestlings from the COPO site cannot presently be explained but may be due to factors that differ between this and the CHIP site. 610 ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 29, NO. 3, 1995
0
3
6
9
12
15
Nestling Age (days) FIGURE 8. Effect of changing PCB concentration in insects on chemical accumulation in nestlings. Simulations were obtained by setting the PCB concentration in the egg equal to loo0 ng g-' (intermediate to levels measured at the CHIP and COPO sites). The residue level in insects was then varied from 100 to 500 ng g-'. All other model parameters were set equal to values given in the text.
One possibility is that the percentage of the diet derived from emergent insects varied between sites. The direct observations necessary to evaluate this possibility are lacking. However, it is clear that a substantial reduction in this parameter (from to 70% to 30%)would be required to "explain"the observed result. Alternatively,it is possible that chemical assimilation efficiency from the diet varies at the two sites, although this seems unlikely since the concentration gradient driving chemical diffusion into the
bird should be higher in nestlings from the COPO site. The bioenergetics description for nestling swallows also represents apotential source of error in model simulations. In particular, the predicted amount of food consumption required to support the growth of a 15-d old nestling (C productionlC consumption, generally referred to as energy conversionefficiency;Table 2) is greater than that estimated for other passerine birds. An increase in energy conversion efficiency would result in lower residue concentration estimates by reducing the amount of insects that birds eat. Moreover, the impact of a change in this parameter would be greater for birds from the COPO site than for those from the CHIP site. This is because insects represent a relatively greater contribution (compared to inherited residues) to final residue values in chicks from the more contaminated site. Efforts to obtain an independent estimate of the consumption term for tree swallows were complicated by the fact that published estimates for other passerine birds did not present a clear pattem. The consumption equation was therefore parameterized by fitting model simulations to observed growth data. This effort may have resulted in erroneous parameter estimates. However, because the consumption parameter terms were fitted, a change in these values would require correspondingchanges in one or more of the “representative”bioenergetics parameters obtained from the literature if a close fit to observed growth data is to be maintained. Residue data did not provide any evidence for metabolism of individual congeners. Within sites, the correspondence between observed and predicted residues was similar for all congeners examined. Model predictions for PCB 101 were of particular interest because this pentachlorobiphenyl is thought to represent a class of congeners (meta-para-unsubstituted) that can be metabolized by birds (57, 58). When injected into eider ducklings at low concentrations, the half-life of PCB 101 was found to be approximately 16 d. At higher concentrations, however, the half-life increased to over 100 d, presumably due to saturation of a rate-limiting step for elimination (58). Due to the short time span of the nestling development period and to other sources of variability in residue values, it is unlikely that metabolism would have a discernible impact on observed residues unless the half-life for elimination by this route was short-perhaps 30 d or less. As noted previously, metabolism data for birds are limited and are essentially nonexistent for very young animals. This information is required if bioenergetics-based models are to be developed for compounds that undergo significant metabolic biotransformation. Model simulations and measured residues both suggest that PCB concentrations are lower during the growth dilution phase of nestling development than at any other time in the life cycle of the bird. It is interesting, therefore, to note the growing number of reports of adverse effects of PCHs on the young of piscivorous birds. One possible explanation is that effects on young birds originate during the embryonic stage of development. This suggestion is supported by the observation that effects on chicks are often associated with reduced hatching success and increased incidence of congenital abnormalities. In a recent study, however, the development of Forster’s tern chicks from Green Bay, WI, was reported to have been impaired despite an absence of discemible effects on hatching success (8). Because toxicity data are presently lacking, there is no
way to know the relative sensitivity of different life stages of birds to a given dose. In addition, the toxicity of PCBs to young birds may be modified by extrinsic factors such as toxicity to adult birds, resulting in reduced quality of parental care (51. The value of nestling tree swallows as sentinels of local sediment contamination depends in part upon the variability between birds collected from a single site, since this will determine the number of samples that would be required to characterize a site and to make statistical comparisons between sites. Recognizing that at each site residue levels in chicks are affected by a large number of factors apart from the actual extent of contamination (e.g., residue inheritance, foragingbehavior of adults, brood size), the within-site variability in chick residues observed in this study was surprisingly low. The results of the present study suggest, however, that it may be difficult to draw quantitative conclusions about sediment contamination based solely upon contaminant bioaccumulation data from swallows. The variable performance of the model at the two sites examined may have been due to factors intemal to the model. However, a strong possibility exists that observed discrepancies were due to site-specific factors. To the extent that this is true, the interpretation of residue data from a given site may depend upon collection of appropriate supporting information. Additional work is also required to better understand the relationship between chemical residues in sediments and those in emergent insects. Working with samples collected from Lake St. Clair, Gobas et al. (23)reported that, for several PCB congeners, adult mayflies were near chemical equilibrium with the sediments from which they emerged. However, an equilibrium model tended to overestimate observed concentrations of two chlorinated benzenes. The accuracy of bioenergetics-based PCB residue predictions is likely to increase as estimates of critical model parameters improve. Until then, residue data from tree swallows must be interpreted with caution. Caution is also advised when interpreting residue data from other species of birds, since many of the same difficulties are likely to be encountered.
Acknowledgments The authors wish to thank Tom Jones, Jane Keyport, and Kathleen Mohrman for assistance with field work and sample collection; Brian Butterworth for the development of analytical methods; Phil Marquis,Chris Harper, and John Libal for analyses of chemical residues; and Sara Kohlbry for subsequent data analyses. In addition, we would like to thank Dr. Ross Norstrom and Dr. Christine Bishop for their helpful contributions and Dr. John Brazner, Virginia Snarski, and Evelyn Hunt for assistance in reviewing the manuscript.
Glossary a A ACTIV
ASSIM
P ABB
BM BW
allometric constant (unitless) activity (kcal g-l d-l) activity coefficient (unitless) efficiency of PCB assimilation from the diet (unitless) allometric exponent (unitless) rate of PCB accumulation (ug bird-’ d-l) basal metabolism (kcal g-l d-l) body weight (g)
VOL. 29. NO. 3. 1995 / ENVIRONMENTAL SCIENCE &TECHNOLOGY
61 1
C
CDB CDI FU
G P R
RMR SDA
TME TR
food consumption rate (kcal g-1 d-1) caloric density of the bird (unitless) caloric density of insect prey (unitless) energy lost due to egestion of feces and excretion of nitrogenous waste (kcal g-l d-l) growth rate (g g-I d-l) production, including tissue growth and fat storage (kcal g-' d-l) total respiration rate (kcal g-l d-l) resting metabolic rate, including basal metabolism, thermoregulation, and specific dynamic action (kcal g-l d-l) specific dynamic action (kcal g-l d-l) total metabolizable energy (kcal g-' d-l) energy expended for thermoregulation (kcal g-' d-l)
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Received f o r review April 28, 1994. Revised manuscript received November 3, 1994. Accepted November 30, 1994.@
ES940267W @Abstractpublished in Advance ACS Abstracts, January 1, 1995.
