Environ. Sci. Technol. 2006, 40, 5624-5628
Adjusting for Temporal Change in Trophic Position Results in Reduced Rates of Contaminant Decline C R A I G E . H E B E R T * ,† A N D D. V. CHIP WESELOH‡ Environment Canada, Canadian Wildlife Service, National Wildlife Research Centre, 1125 Colonel By Drive, Ottawa, Ontario, K1A 0H3, Canada, and Environment Canada, Canadian Wildlife Service, Ontario Region, 4905 Dufferin Street, Downsview, Ontario, M3H 5T4, Canada
The development of ecological tracers to track the flow of energy and nutrients through food webs has provided new insights into the factors that are important in regulating diet composition in wildlife. The Great Lakes Herring Gull Monitoring Program has provided information regarding temporal trends in levels of bioaccumulative contaminants since the early 1970s. In recent years, data from this program have also been generated to examine ecological changes in the Great Lakes. Because the contaminants that are evaluated as part of this program biomagnify, food is the primary determinant of contaminant concentrations in the eggs that are analyzed annually. Fluctuations in diet composition could affect the interpretation of temporal trends by affecting exposure to contaminants. Retrospective analyses involving ecological tracers, i.e., stable nitrogen isotopes and fatty acids, have shown temporal change in the diets of Great Lakes herring gulls at some monitoring colonies. These dietary differences have led to temporal variation in the trophic position of herring gulls. Given that higher trophic level organisms incur greater exposure to biomagnifying contaminants, it is necessary to adjust for these temporal changes in trophic position to get an accurate indication of how contaminant burdens are changing within the Great Lakes ecosystem. Here, we outline a method to adjust for temporal changes in indicator species trophic position and discuss how these adjustments affect the interpretation of contaminant temporal trend monitoring data.
Introduction Accurate estimations of temporal trends in levels of persistent organic pollutants (POPs) are important in evaluating progress toward the elimination of these compounds from the world’s ecosystems. One approach to accomplishing this is through the evaluation of data from biological monitors. Use of high trophic level species to monitor trends in POPs has been widely adopted because these species biomagnify such contaminants, facilitating chemical analysis. They also incur higher chemical exposures relative to lower trophic level species and are, therefore, useful as indicators of POP * Corresponding author phone: (613) 998-6693; fax (613) 9980458; e-mail:
[email protected]. † Environment Canada, Canadian Wildlife Service, National Wildlife Research Centre. ‡ Environment Canada, Canadian Wildlife Service, Ontario Region. 5624 9 ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 40, NO. 18, 2006
effects. However, one of the complicating factors associated with using high trophic level species is that their trophic position is regulated by food web structure (1). If the trophic position of available prey changes through time, then the trophic position of the monitoring species would also be expected to change. This tracking of prey resources has important implications for the interpretation of data from programs monitoring temporal trends in persistent, biomagnifying contaminants because changes in indicator species trophic position would also alter exposure to contaminants. Reduced indicator species trophic position would result in reduced exposure and accumulation of POPs. Such a situation could lead to an overestimation of declines in contaminant levels in the environment. To avoid this situation, a better understanding is required of the exposure dynamics of indicator species as they are regulated by pathways of energy transfer through food webs. The application of ecological tracers can assist in this regard. Ecological tracers are stable chemical and biochemical compounds that can be used to trace the flow of energy and nutrients through food webs. Examples include: stable isotopes, fatty acids, and amino acids (see 1). Herring gulls (Larus argentatus) have been used to monitor contaminant levels and effects in the Great Lakes since 1974 (2, 3). Annual data regarding POP levels in eggs have been extremely important in evaluating the degree to which remedial measures have been successful in reducing the bioavailability of chemical contaminants in the Great Lakes ecosystem. Diet composition is an important factor regulating exposure to biomagnifying contaminants. Spatial differences in the diets of Great Lakes herring gulls have been recognized using traditional means (e.g., analysis of pellets/regurgitations) (4, 5). However, in recent years there has been growing evidence that the food webs herring gulls integrate may have changed in some areas (6, 7). Through the application of specific ecological tracers, i.e., stable nitrogen isotopes and fatty acids, spatial differences in the diets of Great Lakes herring gulls have been confirmed (1). Temporal changes have also been observed, particularly on Lake Erie (1, 6). The degree to which fish were consumed was likely a primary factor regulating the trophic position of herring gulls within the Great Lakes. Utilization of ecological tracers has supplied the means to quantitatively evaluate dietary changes in Great Lakes herring gulls (1). Stable nitrogen isotopes (15N/14N) were used to estimate herring gull trophic position, and fatty acid data provided insights into the degree to which aquatic foods, namely fish, were being consumed (1). As the amount of aquatic food in the gull diet increased (as inferred from increased omega 3/omega 6 fatty acid ratios) the trophic position (δ15N) of the birds also increased. Inter-year differences in δ15N values were likely the result of annual differences in the relative consumption of aquatic versus terrestrial foods. Further insights into how diet regulated trophic position were obtained by examining levels of individual fatty acids associated with particular food types. Omega 3 fatty acids, such as eicosapentaenoic acid (C20:5n-3), are found in the greatest amounts in fish. Eggs containing greater levels of these fatty acids reflected greater consumption of fish. Gulls occupying higher positions were consuming fish to a greater degree. This stemmed from the fact that fish occupy higher trophic levels than other foods that gulls consume (7). Because of biomagnification, fish are, therefore, more contaminated with POPs than other foods, e.g., human refuse (8). If the consumption of fish by herring gulls declines, then exposure to POPs would also be expected to decline. Understanding 10.1021/es0520621 CCC: $33.50
Published 2006 by the Am. Chem. Soc. Published on Web 06/30/2006
this emphasizes the importance of adjusting organochlorine data for changes in trophic position to ensure the correct interpretation of POP temporal trends. Declines in gull trophic position could result in an overestimation of the degree and rate at which POP burdens in the environment are declining. In this study, we examine the impact of trophic position change on the interpretation of POP temporal trend data inferred from the analysis of herring gull eggs. We place particular focus on polychlorinated biphenyl (PCB) trends because of their toxicological significance. In Lake Erie, however, we also examine trends in other important POPs.
Materials and Methods Egg Collection and Storage. Details regarding egg collections are given elsewhere (2). Briefly, 13 herring gull eggs were collected annually from 15 colonies on the Great Lakes as part of Environment Canada’s Great Lakes Herring Gull Monitoring Program (GLHGMP). The location of these monitoring colonies is shown in Hebert et al. (1). For each year at each colony, these samples were pooled on an equal weight basis. Subsamples of whole egg homogenate pools were stored at -40 °C or lower. Annual pooled samples were used for ecological tracer and contaminant analyses. Stable Nitrogen Isotope Analysis. Stable nitrogen isotopes were measured in herring gull egg pools from each of the 15 GLHGMP colonies during 1974-2003. Samples were not available from every year. Details regarding isotope analysis have been described previously (8). Organochlorine Analysis. Annual pooled egg samples collected from all 15 monitoring colonies from 1974 to 2003 were analyzed for dichlorodiphenyldichloroethylene (DDE), dieldrin, heptachlor epoxide (HE), hexachlorobenzene (HCB), mirex, and total PCBs (PCB). To ensure that data were comparable through time, total PCB concentrations used in this analysis were 1:1 Aroclor 1254:1260 estimates (8). Data for 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) were only available from 1984 onward. Details regarding organochlorine analyses are available elsewhere (9, 10). Percent lipid in these egg pools was measured gravimetrically. Statistical Analysis. To evaluate changes in gull trophic position, temporal changes in egg δ15N values were examined using linear regression analysis (11). Annual δ15N values were regressed against annual loge transformed organochlorine concentration data. The residuals from these regressions represented annual organochlorine concentrations adjusted for trophic position. Temporal trends in unadjusted and adjusted organochlorine concentrations were compared. At colonies where there were no significant temporal trends in egg δ15N values, we expected that there would be little difference in organochlorine temporal trends estimated using unadjusted and adjusted data. Temporal trends for PCBs were examined at all 15 annual monitoring colonies. In addition, on Lake Erie, temporal trends in DDE, dieldrin, HE, HCB, mirex, and TCDD were also examined using both unadjusted and adjusted data. To examine temporal trends in contaminant levels, a first-order linear equation was used,
Y)R-β×x Y is the ln contaminant concentration at time x, R is a constant, β is the slope of the contaminant/time regression. Annual percent change in contaminant concentration was calculated as the slope (shown in Tables 1 and 2) of the time/ contaminant regression equation.
Results and Discussion δ15N data from 10 of 15 herring gull monitoring colonies showed a significant temporal decline. These included colonies on all the Great Lakes except Lake Michigan. Significant declines were observed on Lake Superior (Granite
TABLE 1. Temporal Trends in Egg PCB Concentrations at 15 Herring Gull Monitoring Colonies.a unadjusted data
adjusted data
colony
r
p
slope
r
p
slope
% rate
Granite Agawa Gull Big Sister Double Chantry C Shelter Fighting Middle P. Colborne Niagara Hamilton Toronto Snake Strachan
-0.87 -0.87 -0.65 -0.79 -0.91 -0.93 -0.72 -0.90 -0.90 -0.97 -0.93 -0.91 -0.96 -0.91 -0.88
0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001
0.0698 0.0668 0.0447 0.0619 0.0816 0.0982 0.0404 0.0792 0.0480 0.0991 0.0915 0.0754 0.0997 0.0810 0.0721
-0.63 -0.77 -0.64 -0.75 -0.30 -0.88 -0.47 -0.72 -0.56 -0.59 -0.79 -0.71 -0.69 -0.48 -0.86
0.001 0.0001 0.0001 0.0001 0.123 0.0001 0.027 0.0001 0.002 0.002 0.0001 0.021 0.0001 0.014 0.0001
0.0454 0.0571 0.0439 0.0588 0.0156 0.0848 0.0231 0.0522 0.0218 0.0411 0.0723 0.0467 0.0534 0.0250 0.0685
65 86 98 95 19 86 57 66 45 41 79 62 54 31 95
a Trends were calculated using unadjusted (ln-transformed concentrations) and adjusted data (ln-transformed concentrations adjusted for temporal change in gull trophic position). % rate is the relative rate of temporal decline of the adjusted data relative to the unadjusted data. Colonies in bold were those that exhibited a significant temporal decline in trophic position as inferred from egg δ15N values. See text for details.
I. r ) -0.69, p ) 0.001; Agawa Rocks r ) -0.49, p ) 0.012), Lake Huron (Double I. r ) -0.90, p ) 0.001; Channel/Shelter I. r ) -0.65, p ) 0.001), Lake Erie (including Fighting I. r ) -0.55, p ) 0.005; Middle I. r ) -0.72, p ) 0.001; Port Colborne r ) -0.77, p ) 0.001), and Lake Ontario (including Niagara River r ) -0.50, p ) 0.018; Toronto Harbor r ) -0.67, p ) 0.001; Snake I. r ) -0.78, p ) 0.001). Colonies showing marginally nonsignificant declines (p < 0.1) were Chantry I. in Lake Huron (r ) -0.33, p ) 0.096) and Hamilton Harbor (r ) -0.56, p ) 0.089). There were no statistically significant temporal trends in percent lipid levels in egg pools from 14 of the 15 colonies (Toronto Harbor showed a weak positive increase through time, r ) 0.39, p ) 0.03). Thus, there was no evidence to suggest that changes in total lipid availability were important in regulating the dynamics of contaminant uptake and/or elimination. Annual egg δ15N and PCB values were significantly positively correlated at eight of the 15 colonies (Granite I., Double I. (Figure 1a), Channel-Shelter I., Fighting I., Middle I., Port Colborne, Toronto Harbor, Snake I.). Colonies in the Niagara River (r ) 0.39, p ) 0.08) and Hamilton Harbor (r ) 0.62, p ) 0.06) exhibited marginally nonsignificant correlations between egg δ15N and PCB values. At Middle Island and Port Colborne, annual egg concentrations of DDE, dieldrin, HE, HCB, mirex, and TCDD (Figure 1b) were all correlated with annual egg δ15N values (p < 0.05). Temporal trends in contaminant data adjusted for trophic position were compared with temporal trends in the unadjusted data (Table 1). For unadjusted PCB data, significant temporal declines were noted at all colonies. Using the adjusted data, significant declines were found at all colonies except Double Is. in Lake Huron (r ) -0.30, p ) 0.123) (Figure 2). In addition, at colonies where there were significant temporal declines in egg δ15N values (10 of 15 colonies), adjusted PCB levels showed a less pronounced temporal decline (estimated using the slope of the regression equations). PCB concentrations, adjusted for changes in trophic position, declined at a mean rate of 54% of the unadjusted PCB data (Table 1). At colonies where there was no significant trend in egg δ15N values (five of 10 colonies) the mean rates of decline calculated using unadjusted and adjusted data were more similar. Rates calculated using adjusted data were 87% of those calculated using the unadjusted data. At Port Colborne, eastern Lake Erie, significant temporal declines in trophic position-adjusted contaminant levels were VOL. 40, NO. 18, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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TABLE 2. Temporal Trends in Egg Organochlorine Concentrations at two Colonies in Lake Erie (Middle I., Western Basin; Port Colborne, Eastern Basin).a unadjusted data contaminant DDE Dieldrin HE HCB Mirex TCDD PCB
adjusted data
colony
r
P
slope
r
p
slope
% rate
Middle P.Colborne Middle P.Colborne Middle P.Colborne Middle P.Colborne Middle P.Colborne Middle P.Colborne Middle P.Colborne
-0.88 -0.96 -0.92 -0.91 -0.91 -0.91 -0.96 -0.96 -0.74 -0.92 -0.79 -0.95 -0.90 -0.97
0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001 0.0001
0.0634 0.1152 0.0789 0.1123 0.0808 0.1089 0.1165 0.1316 0.1029 0.1298 0.0630 0.1563 0.0480 0.0991
-0.61 -0.57 -0.63 -0.47 -0.62 -0.48 -0.69 -0.57 -0.51 -0.53 -0.20 -0.67 -0.56 -0.59
0.001 0.003 0.001 0.02 0.001 0.019 0.0001 0.004 0.01 0.007 0.467 0.005 0.002 0.002
0.0360 0.0461 0.0356 0.0323 0.0335 0.0321 0.0647 0.0541 0.0627 0.0540 0.0096 0.0820 0.0218 0.0411
57 40 45 29 41 29 56 41 61 42 15 52 45 41
a Trends were calculated using unadjusted (ln-transformed concentrations) and adjusted data (ln-transformed concentrations adjusted for temporal change in gull trophic position). See text for details. % rate is the relative rate of temporal decline of the adjusted data relative to the unadjusted data.
FIGURE 1. Annual egg δ15N values were correlated with annual egg contaminant concentrations at many colonies (a) Double Is. (Lake Huron), egg δ15N versus egg PCB concentrations (1974-2003) (b) Middle Is. (Lake Erie), egg δ15N values versus egg TCDD concentrations (1984-2002). observed for all contaminants. However, rates of decline were less than for unadjusted data (Table 2). Rates of decline using trophic position adjusted data were approximately 40% of those calculated using the unadjusted data. At Middle Island, western Lake Erie, significant temporal trends in contaminant levels adjusted for trophic position were observed for all 5626
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FIGURE 2. Temporal trends in egg PCB levels at Double Is., Lake Huron. (A) using unadjusted ln-transformed data (B) using lntransformed data adjusted for temporal change in gull trophic position. contaminants except TCDD (Figure 3). Again, rates of decline using trophic position adjusted data were slower than those calculated using the unadjusted data. Rates of decline estimated using the adjusted data were approximately half of those calculated using the unadjusted data (Table 2). The results reported here emphasize the importance of considering changes in food webs when evaluating temporal change in environmental POP burdens. Rates of decline
Lakes, lake trout (Salvelinus namaycush) is an important biomonitoring species (e.g., refs 12, 13). Its diet has likely changed as a result of alterations in the composition of aquatic communities (e.g., decline of Diporeia hoyi and an increase in exotic invertebrate and fish species). Changes in marine prey fish communities have also occurred, likely resulting in shifts in pathways of energy and contaminant flow to other seabird monitoring species (14). These are only a few examples where the application of ecological tracers could assist in the interpretation of environmental monitoring data. This study demonstrates the usefulness of ecological tracers in understanding pathways of energy flow to high trophic level species. Food web structure is important in determining the flow of energy, nutrients, and contaminants through ecosystems (15). Therefore, improving our ability to define food web structure, recognize change, and account for it are critical to the accurate assessment of temporal trends in environmental contaminant burdens. Here, we present a method to adjust POP data for temporal change in organism trophic position using stable nitrogen isotopes. Changes in trophic position as a result of food web change need to be considered if we are to use such data to accurately evaluate progress in reducing environmental POP burdens. The application of ecological tracers, such as stable nitrogen isotopes, will lead to a better understanding of exposure dynamics in monitoring species and will improve their utility as indicators of environmental quality.
Acknowledgments
FIGURE 3. Temporal trends in egg TCDD levels at Middle Is., Lake Erie. (A) using unadjusted ln-transformed data (B) using lntransformed data adjusted for temporal change in gull trophic position. calculated using the adjusted data were slower than using the unadjusted data. In addition, after adjusting for temporal change in gull trophic position, nonsignificant temporal declines were observed for some contaminants at some monitoring colonies (PCBs at Double Is. Lake Huron; TCDD at Middle Is. Lake Erie). These differences are significant enough to affect the interpretation of the degree to which POP burdens may be changing in the environment. Given the toxicological importance of compounds such as PCBs and TCDD, correct interpretation of the extent to which they are declining is critical for assessing risk to wildlife and humans. This analysis indicates that interpreting POP declines, without accounting for dietary change, results in an overestimation of the degree to which these contaminants have declined in the environment. It should be noted, however, that these results only apply to contaminants that biomagnify (e.g., GLHGMP contaminants: POPs, methyl mercury). Compounds that are efficiently metabolized or inefficiently accumulated will be less affected by changes in indicator species trophic position.Another caveat that needs to be recognized in this analysis is that changes in egg δ15N were solely interpreted as reflecting changes in gull trophic position. It is possible that changes in δ15N values at the base of the food web (see ref 1) could also have played some role in contributing to egg δ15N trends. Clearly, further research is required to evaluate this possibility, but data from Lake Erie do not support this hypothesis (1). The potential impact of food web changes on the interpretation of contaminant monitoring data is not likely to be an issue that is unique to the GLHGMP. Change in food web structure is a widespread phenomenon. In the Great
K. Hobson’s (CWS, Prairie and Northern Region) laboratory in Saskatoon conducted the stable isotope analyses. We thank Birgit Braune, Shane DeSolla, Karen Keenleyside, Ross Norstrom, Nancy Patterson, Cynthia Pekarik, Laird Shutt, and three anonymous reviewers for their comments on an earlier version of this manuscript. Environment Canada’s Great Lakes Action Plan supported this research.
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(10) Won, H. T.; Mulvihill, M. J.; Wakeford, B. J. Multiresidue methods for the determination of chlorinated pesticides and polychlorinated biphenyls (PCBs) in wildlife tissues by gas chromatography/mass spectrometry; Technical Report Series no. 335E; Canadian Wildlife Service, National Wildlife Research Centre: Hull, Quebec, Canada, 2001. (11) StatSoft Inc. STATI STICA data analysis software system, version 7.1; Tulsa, OK, 2005. (12) Luross. J. M.; Alaee, M.; Sergeant, D. B.; Cannon, C. M.; Whittle, D. M.; Solomon, K. R.; Muir, D. C. Spatial distribution of polybrominated diphenyl ethers and polybrominated biphenyls in lake trout from the Laurentian Great Lakes. Chemosphere 2002, 46, 665-672. (13) Whittle, D. M.; Keir, M. J.; Gorrie, J. F.; Murphy, E. State of the Lakes Indicators Report; SOLEC Indicator #121-Contaminants
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in Whole Fish; SOLEC, 2004; pp 128-138. http://www.solecregistration.ca/en/reports/default.asp. (14) Davoren, G. K.; Montevecchi, W. A. Signals from seabirds indicate changing biology of capelin stocks. Mar. Ecol.: Prog. Ser. 2003, 258, 253-261. (15) Morrison, H. A.; Whittle, D. M.; Haffner, G. D. A comparison of the transport and fate of polychlorinated biphenyl congeners in three Great Lakes food webs. Environ. Toxicol. Chem. 2002, 21, 683-692.
Received for review October 18, 2005. Revised manuscript received May 5, 2006. Accepted May 31, 2006. ES0520621
