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1 April 2016 Forty-Year Decline of Organic Contaminants in Eggs of Herring Gulls (Larus argentatus) from the Great Lakes, 1974 to 2013
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Following the discovery of widespread adverse reproductive effects in fish-eating colonial waterbirds nesting in the Canadian Great Lakes, Environment Canada started monitoring contaminants in Herring Gull (Larus argentatus) eggs in 1974. Current and historical concentrations and rates of decline of legacy contaminants (Polychlorinated Biphenyls [PCBs], 2,3,7,8-tetrachlorodibenzo-p-dioxin [TCDD] and organochlorine pesticides) in Herring Gull eggs from 15 Great Lakes colonies over 40 years are reported here. Large declines in contaminant concentrations were found in all colonies from the first year of reporting to 2013, with mean percent declines ranging from 72.7% for Σ chlordane to 95.2% for Mirex, indicating reduced availability of contaminants to wildlife. First-order exponential decay regressions indicated that rates of decline in eggs varied among compounds. Herring Gulls from Strachan Island (St. Lawrence River), for example, had the highest rates of decline for Dieldrin and Hexachlor Epoxide, whereas those from Middle Island (Lake Erie) had the lowest rates of decline for TCDD and PCBs, and those from Gull Island (Lake Michigan) had the lowest rates of decline for HCB and Mirex. Exponential rates of decline in Herring Gulls mirrored those previously reported for Great Lakes fish, thus demonstrating that Herring Gulls are a good fish-eating indicator species.

In the late 1960s, eggs of Herring Gulls (Larus argentatus) in Lake Michigan were discovered to contain elevated concentrations of organic contaminants, and the species was suffering from high embryonic mortality, eggshell thinning and poor reproductive success (Keith 1966). In the early 1970s, some of these same adverse reproductive effects were found to be prevalent in Herring Gulls and other fish-eating colonial waterbirds nesting in Lake Ontario and other areas of the Canadian Great Lakes, and were severely limiting populations of colonial waterbirds (Gilbertson and Reynolds 1972; Gilbertson 1974; Gilbertson and Hale 1974; Gilbertson and Fox 1977). Those studies soon led to the adoption of the Herring Gull and its eggs by the Canadian Wildlife Service-Environment Canada as an indicator species of health and contaminant exposure for fish-eating wildlife in the Great Lakes (Gilman et al. 1977; Fox et al. 1978); therefore, the Great Lakes Herring Gull Monitoring Program (GLHGMP) was born and continues to this day.

The Herring Gull is an excellent indicator species for organic contaminants on the Great Lakes. It breeds on all five of the individual lakes, including most connecting channels, and its eggs are relatively high in lipid content where many contaminants accumulate. Herring Gulls are primarily fisheaters and therefore have a relatively high exposure to lipophilic contaminants (Weseloh 2012). They are relatively resistant to effects of contaminants and, as such, it takes very elevated concentrations of contaminants to cause adverse health effects in the species (Weseloh 2012). Adult Herring Gulls are non-migratory on the Great Lakes and therefore only reflect contaminants from the Great Lakes (Weseloh 2012). Lastly, they are well-studied and well-known to the public.

In its current form, the GLHGMP has three different components: 1) the tracking of temporal and spatial trends of various contaminants in eggs (and other tissues) of Herring Gulls (Norstrom et al. 2002; Gauthier et al. 2008; Weseloh et al. 2011); 2) contaminant-related effects on the health, physiology and genetics of Herring Gulls (Rutkiewicz et al. 2010); and 3) the search for new emerging contaminants in the Great Lakes ecosystem (Gauthier et al. 2007; Letcher et al. 2015; Su et al. 2015). The entire program was reviewed (Hebert et al. 1999), which assessed how successful the program has been in achieving its main goals. Lastly, although not an integral part of the program, the GLHGMP has proved valuable in contributing to our understanding of food web dynamics and the importance of understanding diet in interpreting contaminant and related data (e.g., Hebert et al. 1999, 2008; Hebert and Weseloh 2006).

A very practical application of all three of the program's components is to assess environmental problems that have impaired wildlife, such as in Great Lakes Areas of Concern (AOCs), as well as sites that are not AOCs (Weseloh et al. 1995). The 1987 Protocol to the 1978 Great Lakes Water Quality Agreement has committed both Canada and the United States to the “virtual elimination of persistent toxic substances” (International Joint Commission 1988). Forty-three areas in the Great Lakes-St. Lawrence basin were designated as AOCs based on impairment of beneficial uses and the inability of the regions to support healthy aquatic life (International Joint Commission 1988). Delisting of AOCs is dependent upon the remediation of the causes of beneficial use impairments. Several Herring Gull colonies are monitored within or near the boundaries of AOCs that include Cornwall, Toronto, Hamilton, and Detroit River; the data collected on health and contaminant burdens are used to evaluate beneficial use impairments that pertain to wildlife.

Previous publications have dealt with similar data for earlier time periods on a lake by lake basis or for a specific AOC (e.g., Weseloh et al. 1990, 1994, 2005), as well as on a Great Lakes-wide basis (e.g., Hebert et al. 1994; Pekarik and Weseloh 1998; Weseloh et al. 2006). Many past temporal analyses of contaminants in gull (Laridae) eggs or other biota used log transformed linear regressions, or similar permutations of linear regression, or used “equilibrium lipid partitioning concentrations” to express concentrations of PCBs in air, water, sediments, fish, and Larid eggs on a common equilibrium partitioning basis. Webster et al. (1999) used first order exponential decay models for determining trends for Lake Ontario and Lake Superior. Furthermore, because most of the mass of PCBs and most other legacy persistent organic pollutants (POPs) in the environment are contained in sediments and soils, and because temporal trends in these substrates after POP production ceased generally follow first order decay models (Van Metre et al. 1998; Ayris and Harrad 1999; Sinkkonen and Paasivirta 2000), one would expect that trends in biota would similarly follow exponential decay models. Therefore, our objective, which deals with the first component of the GLHGMP, is to report on current and historical concentrations as well as changes in rates of decline, or stabilization, of legacy contaminants (Polychlorinated Biphenyls [PCBs], 2,3,7,8-tetrachlorodibenzo-p-dioxin [TCDD], and organochlorine pesticides) in Herring Gull eggs following 40 years of monitoring from the early 1970s to 2013.


Egg Collection

Herring Gull eggs have been collected annually as part of the GLHGMP at 15 Herring Gull colonies throughout the Great Lakes and connecting channels since as early as 1974 (Weseloh et al. 2011). Colony names and locations are: Granite Island (48° 43′ 12.39″ N, 88° 27′ 32.04″ W) and Agawa Rocks (47° 21′ 32.04″ N, 84° 41′ 35.88″ W) on Lake Superior; Gull Island (45° 42′ 36.41″ N, 85° 50′ 17.51″ W) and Big Sister Island (45° 13′ 26.65″ N, 87° 8′ 48.22″ W) on Lake Michigan; Chantry Island (44° 29′ 19.67″ N, 81° 24′ 9.57″ W), Double Island (46° 10′ 24.54″ N, 82° 51′ 45.93″ W), and Channel-Shelter Island (43° 40′ 12.24″ N, 83° 49′ 23.04″ W) on Lake Huron; Fighting Island (42° 11′ 27.11″ N, 83° 6′ 52.43″ W) on the Detroit River; Middle Island (41° 40′ 54.01″ N, 82° 40′ 54.12″ W) and the Port Colborne Breakwater (42° 52′ 5.99″ N, 79° 15′ 29.88″ W) on Lake Erie; Weseloh Rocks (43° 4′ 31.55″ N, 79° 4′ 12.65″ W) on the Niagara River; Neare and North Islands and Eastport Pier 27 in Hamilton Harbour (~43° 18′ 9″ N, 79° 48′ 9″ W), Leslie Street Spit in Toronto Harbour (43° 37′ 19.25″ N, 79° 20′ 25.95″ W) and Snake Island (44° 11′ 26.81″ N, 76° 32′ 35.61″ W) on Lake Ontario; and Strachan Island (45° 1′ 15.45″ N, 74° 48′ 43.36″ W) just above the dam at Cornwall, Ontario, on the St. Lawrence River (Fig. 1). Eggs were collected annually from each colony generally from 1974 to 2013, usually during late April-early May; dates of first egg collection are summarized in Table 1. With some exceptions, for each year, a single egg was collected from one of 9–13 freshlyincubated Herring Gull clutches and then either analyzed as individual eggs (1974–1985) for which annual means were calculated or pooled for a single chemical analysis (1986 to present). Eggs were collected soon after the last egg was laid and clutches with two or fewer eggs were generally not targeted for egg collection. From each clutch, an egg was haphazardly collected; therefore, eggs were not biased toward eggs of a certain size or order of laying. After collection, egg contents were placed in acetone- and hexane-rinsed amber jars and frozen prior to chemical analysis. Furthermore, eggs were not collected from Fighting Island post-2010 because no breeding colonies were found on the Canadian side of the Detroit River.

Figure 1.

Herring Gull annual monitoring colonies in the Great Lakes and connecting channels, 1974–2013.


Chemical Analyses

From the early 1970s to 1985, individual eggs from collections were analyzed for PCBs and other organochlorine pesticides at the Ontario Research Foundation - currently Process Research ORTECH Inc. - in Mississauga, Ontario, using high resolution gas chromatography-electron capture detection (GC-ECD; Reynolds and Cooper 1975; Norstrom et al. 1980). Concentrations of PCBs were expressed as a mixture of Aroclor 1254:1260 (1:1) and estimated by a single peak corresponding to PCB 138 (Turle et al. 1991). Starting in 1986, egg samples were analyzed as pooled samples at the National Wildlife Research Centre in Ottawa. PCBs and other organochlorines were quantified by GC-ECD for egg samples collected from 1986–1996 and then by gas chromatography with mass selective detection for egg samples collected from 1997–2013. For further details of chemical methods, see de Solla et al. (2010). To allow comparisons with earlier data, PCBs were expressed as Aroclor 1254:1260 1:1 equivalents. Due to space limitation, we report on concentrations of the six most abundant organochlorine pesticides or metabolites found in eggs. These include the contaminants that contributed the most to the ranking of Great Lakes colonies based on their concentrations relative to exceedances of fish flesh criteria for the protection of piscivorous wildlife (Weseloh et al. 2006): 1,1-bis-(4-chlorophenyl)-2,2-dichloroethene (p,p'-DDE), Dieldrin, Mirex, Σ chlordane (as the sum concentration of cis, trans, oxy-chlordane, cis- and trans-nonachlor), Hexachlorobenzene (HCB), and Heptachlor Epoxide (HE). Minimum detection limits (MDLs) for organochlorine and chemical analyses ranged between 0.0001 μg/g to 0.005 μg/g. Although changes in analytical methods used to quantify compounds during the study period could influence reported trends (de Solla et al. 2010), we were unable to create adjustment methods for the earlier data from 1974 to 1985, so we used unadjusted data. Gas chromatography/mass spectrometry was used to measure TCDD in Herring Gull eggs beginning in 1981 (Norstrom and Simon 1991; Simon and Wakeford 2000). All samples were above MDLs for TCDD, which ranged from 0.1–2 pg/g. Spikes, duplicates, blanks, and certified reference material were analyzed concurrently with the Herring Gull eggs and met quality assurance standards.

Statistical Analyses

Past analyses of temporal trends of contaminants in Herring Gull eggs used either log transformed linear regressions or change point regressions, which are also linear regressions (e.g., Norstrom et al. 2002; Hebert and Weseloh 2006; Weseloh et al. 2006; de Solla et al. 2010). In this study, we examined exponential decay models and calculated both decay constants and halflives for compounds at all colonies to assess temporal trends. Regressions were performed using arithmetic means, where individual analyses of eggs were conducted, or as single values for pooled eggs. Earlier studies have determined that single values of pooled samples are equivalent to the mean concentrations calculated from the same eggs analyzed individually (Turle and Collins 1992). Regressions were used to assess temporal trends of contaminants in Herring Gull eggs; using both linear regressions of ln transformed contaminant concentrations, and by using a first-order exponential decay model:

where Ct is the concentration at time t, C0 is the concentration at the first year that data were reported, λ is the decay constant (where the concentration decreases at a rate proportional to its current value), and e is Euler's constant. The first year that egg collections were performed and reported at a Great Lakes colony was considered as t = 1. To compare decay constants among colonies or contaminants, 84% confidence intervals were calculated. When comparing decay constants among colonies, statistical significance was assessed as a nonoverlap of confidence intervals of the decay constants among treatments. A confidence interval of 84% was used because this confidence interval is approximately equivalent to the nominal α = 0.05 when using frequentist tests, assuming that the ratio of the two confidence intervals are one (Payton et al. 2003). The farther the ratio is from one, the smaller the discrepancy between the nominal value of α = 0.05 and the actual α; as the ratio approaches ∞, the discrepancy between the nominal and actual α approaches zero. Contaminant half-lives were calculated as:
Analyses were completed using STATISTICA software (StatSoft, Inc. 2004) with a significance level of α = 0.05.


Burdens of POPs in eggs of Herring Gulls have declined considerably at all colonies from the 1970s or early 1980s to 2013 (Table 1). Concentrations of PCBs (Aroclor 1254:1260 1:1 equivalents), for example, ranged between 50.1 and 165.6 μg/g among the 10 colonies monitored in the early 1970s, whereas by 2013 the highest value was 14.8 μg/g. Similar trends were observed for the organochlorine pesticides. Mirex declined the most overall, with concentrations in 2013 that were on average only 4.9% of the concentrations in the year of first reporting (Table 2). For all contaminants, the regression slopes were significantly less than 1 (all P ≤ 0.05) for all colonies, and the mean percent declines from the first year of reporting to 2013 ranged from 72.7% for Σ chlordane to 95.1% for Mirex (Table 2). The colony that had the largest overall percent decline for all contaminants was Big Sister Island (Lake Michigan), with an average decline of 96.4%, whereas Leslie St. Spit (Toronto Harbour) had the lowest overall decline of 82.1%. For Aroclor 1254:1260 1:1 Middle Island had the lowest rate of decline; it had a significantly greater decay constant (i.e., lower rate of decline) compared to all other colonies, with the exception of Channel-Shelter Island (Lake Michigan).

When using linear regressions of ln transformed contaminant data, it was clear that, even for transformed data, rates of decline were not constant across years for all contaminants or colonies. By visually examining the data, in many cases it appeared that the rates of decline diminished in later years. We calculated change point regressions, with 2003 as a change point, for all comparisons, and compared the slopes before and after 2003. For 40% of the comparisons (9 contaminants × 15 colonies), the slopes from 2003 onward were significantly greater (less negative) than the slopes from the first year of reporting to 2002. In general, the temporal trends in contaminants better fit an exponential decay model, rather than a combination of single or break point linear regressions. As an example, the temporal trend for Aroclor 1254:1260 1:1 in Herring Gull eggs from Port Colborne shows different rates of decline from 1974 to 2002 compared to 2003 and onward, which could be better explained using two linear regressions (Fig. 2A). However, the first order exponential decay exhibited a better fit overall (Fig. 2B). It was not always the case; HE did not fit any distribution particularly well for Big Sister Island, including exponential decay.

Table 1.

Concentrations of Polychlorinated Biphenyls (PCBs) and organochlorine pesticides (μg/g, wet weight) and 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) (pg/g, wet weight) in Herring Gull eggs from the Great Lakes in the first and last years of reporting. Data shown represent either an arithmetic mean concentration for individual eggs or a single concentration for a pooled sample of eggs. DDE = 1,1-bis-(4-chlorophenyl)-2,2-dichloroethene; HE = Heptachlor Epoxide; HCB = Hexachlorobenzene.




Decay constants varied among colonies for each contaminant (Table 2). Strachan Island, for example, had the largest decay constants (i.e., had the highest rate of decline) for Dieldrin and HE, whereas Middle Island had the smallest decay constants for TCDD and PCBs, and Gull Island had the smallest for HCB and Mirex. For all contaminants, the colonies that had the fastest and slowest rates of decline had decay constants that were significantly different from each other (Table 2). In some cases, such as for Aroclor 1254:1260 1:1 at Big Sister Island and Middle Island, Big Sister Island initially had higher concentrations in eggs compared to those from Middle Island, but by the late 2000s the situation had reversed (Table 1). Mean halflives for all colonies combined ranged from 5.5 to 13.7 years for PCBs, TCDD and the six organochlorines. For Σ PCBs, the half-lives ranged from 9.9 to 24.3 years among colonies, with Middle Island having the longest half-life. Overall, Middle, Granite and Gull islands had the longest half-lives for POPs.


At all colonies of Herring Gulls monitored in the Great Lakes, concentrations of PCBs and organochlorine pesticides have fallen dramatically since the 1970s. We found that, in general, trends in contaminant burdens followed an exponential decline from the 1970s to 2013, i.e., the rate of decline was proportional to the concentration at that time. Many other studies, primarily on fish, have found similar results for the Great Lakes region. Gewurtz et al. (2011) found that PCBs and total 1,1′-(2,2,2-trichloroethane-1,1-diyl)bis(4-chlorobenzene) (DDT) concentrations in fillets of lake trout (Salvelinus namaycush) and lake whitefish (Coregonus clupeaformis) from Lake Simcoe, Ontario, declined exponentially, but stabilized in the 1990s. Hickey et al. (2006) also found, using both single and double exponential models, that concentrations of PCBs and organochlorine pesticides initially declined in Great Lakes lake trout and walleye (Sander vitreus), but that there was a stable contaminant source resulting in more constant trends in later years. Prior to 1980, the halflife of PCBs was 2 years, but after 1980 the half-life was 13.6 years (Hickey et al. 2006). Sadraddini et al. (2011) also used a variety of exponential decay models to estimate contaminant trends in fish and found that PCB concentrations in walleye increased after the mid-1990s from Lake Erie. Similar trends have been observed outside of the Great Lakes. Because fish in the Great Lakes are showing such patterns of decline in POPs, it is not surprising that the contaminant body burdens of a primarily fish-eating bird — the Herring Gull — also exhibited a similar pattern of decline in the Great Lakes.

Table 2.

Mean percent declines (SD), mean decay constants (SD) and mean half-lives (SD) for Polychlorinated Biphenyls (PCBs), organochlorine pesticides and 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in Herring Gull eggs from 15 Great Lakes colonies from the first year of reporting to 2013 (with the exception of Fighting Island where the last year of reporting was 2010). Minimum and maximum values and associated colonies are also shown. Note that colonies identified with the smallest (minimum) decay constant also have the longest (maximum) half-life and vice versa. DDE = 1,1-bis-(4-chlorophenyl)-2,2-dichloroethene; HE = Heptachlor Epoxide; HCB = Hexachlorobenzene; I = Island.


Figure 2.

Temporal changes in concentrations of PCBs (Aroclor 1254:1260 1:1 equivalents; μg/g ww) in Herring Gull eggs from Port Colborne, 1974–2013. A breakpoint regression (A) ln transformed and exponential decay (B) regression was used to elucidate the nature of the decline in concentrations.


The rates of decline in POPs in Herring Gull eggs are generally lower in later years, and for many colonies, concentrations have stabilized in the last few years (Fig. 3). The colony that had the lowest rate of decline for PCBs and TCDD was Middle Island, which is downstream of the Detroit River. In another contaminants study, mean concentrations of PCBs in caged eastern elliptio mussels (Elliptio complanata) in the Detroit River from 1996 to 2010 revealed that although PCBs had declined between 2003 and 2010 at one monitoring site, burdens in mussels showed no trends at two sites and even had increasing trends at one site (Drouillard et al. 2013). Reasons for the stabilization or even slight increase in PCB burdens in Herring Gull eggs from the Detroit River or western Lake Erie are unknown, but may be related to resuspension of PCBs from contaminated sediment along the Detroit River. Similar long term declines in PCBs and other organochlorines in suspended sediment and fish from the Great Lakes have been reported since the 1970s/1980s (Gewurtz et al. 2011; Drouillard et al. 2013). Mercury in Herring Gull eggs from the Great Lakes have shown similar temporal trends to POPs; Weseloh et al. (2011) found that although overall mercury concentrations declined in Herring Gull eggs from 1974 to 2009, there were few changes in concentrations in the last 15 years of their study. Similarly, concentrations of mercury in walleye and northern pike (Esox lucius) generally increased (0.01–0.27 μg/g per decade) between 1995 and 2012 in Ontario (Gandhi et al. 2014).

Although we found dramatic declines in contaminant burdens, not all of these changes are due solely to the elimination of the contaminants in the environment. Changes in food web components may affect exposure to contaminants and body burdens in wildlife. If Herring Gulls switch to feeding lower in the food web, their rate of contaminant intake, and thus the contaminant load in their eggs, would decline. Bunnell et al. (2014) suggested that in many of the Great Lakes, there has been an increase in water clarity concurrent with declines in phytoplankton, invertebrates (excluding invasive species), and prey fish. Declines in prey fish were most obvious in the upper Great Lakes. By using stable isotopes and essential fatty acids, Hebert and Weseloh (2006) found that not only did Herring Gull diets and trophic level change at many Great Lakes colonies between 1974 and 2003, but when the effect of changing trophic level was removed, rates of contaminant declines were reduced. Unless researchers conducting monitoring programs are aware of a change in food web structure, they will, in this situation, overestimate the long term temporal declines in PCBs and organochlorine pesticides in fisheating birds (Hebert and Weseloh 2006; Hebert et al. 2008). In actual fact, the Herring Gulls have only switched to eating a cleaner food source; therefore, the actual change in contaminants in the food web is likely lower than what we found, due to the confounding effect of the change in diet.

Not only has the fish community changed in the Great Lakes, but the food quality may have changed as well. Neff et al. (2012) found that lipid content has declined, in general, in the muscle of commercial fish over a 35-year period. Therefore, not only may the energetic (and presumably nutritional) composition of fish have changed in the Great Lakes, but because POPs sequester primarily in the lipids of animals, changes in lipid composition in fish may have altered the partitioning of POPs in the food web. Measurements of body burdens in wildlife integrate the net effect of factors such as bioavailability, temperature, growth rates, food chain dynamics, and chemical partitioning behavior, among others.

Figure 3.

Temporal changes (exponential models) in concentrations of PCBs (Aroclor 1254:1260 1:1 equivalents) and six organochlorine pesticides (μg/g, wet weight) and 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) (pg/g, wet weight) in Herring Gull eggs from the Great Lakes, 1974–2013. For each compound, data were reported for the two colonies that had the highest (fi01_166.gif) and lowest (fi02_166.gif) decay constants.


The mechanisms behind the manner in how these legacy POPs are declining are not established. The degree that factors such as degradation, metabolism, loss via atmospheric or aqueous transport, sequestering in specific environmental compartments, or changes in food web dynamics are driving the changes is not known. Nonetheless, exponential models are often assumed when estimating rates of decline of legacy POPs in abiotic compartments (e.g., Mackay et al. 1994). Van Metre et al. (1998) found that trends in concentrations of PCBs and total DDT decreased exponentially from the 1960s to 1990s in sediment cores taken from riverine systems, and suggested a first-order decay rate process. The rates of elimination of body burdens for POPs are much faster than the rates of environmental degradation; hence changes in body burdens reflect changes in the bioavailability of POPs. Degradation half-lives of tri- to hepta-chlorinated PCBs in sediment were estimated to range between 3 and 38 years, with the congeners frequently found in Herring Gull eggs having half-lives of 10 to 19 years in sediment (Sinkkonen and Paasivirta 2000). Conversely, the half-life of p,p'-DDE in Herring Gulls was estimated to be 264 days (Norstrom et al. 1986), with half-lives for PCBs likely to be similar. Hence, Herring Gulls respond faster to inputs of POPs through their diet than the degradation rate of POPs in the general environment. Abiotic factors, such as global emissions or atmospheric transport, climate change, and local geochemistry may also affect bioavailability of POPs to Larids, and thus their response time and magnitude of changes in burdens (e.g., Gandhi et al. 2014).

Regardless, the main determinant in the declines we observed in Herring Gull eggs is likely the availability of POPs. Although PCBs and organochlorine pesticides are very persistent, they may become increasingly unavailable to fish-eating birds, either through degradation, or by sequestering into environmental compartments that are no longer available for exposure to the food web, such as being buried in sediment. Ultimately, declines in the body burdens of these compounds can be attributed to bans in the production and severe restrictions on the use of these chemicals, improved industrial practices and the effectiveness of remedial activities such as dredging and disposal of contaminated substrates, thereby reducing the chemical inputs into the environment. Despite bans in production, the persistent nature of these compounds means that they continue to be available and accumulate in biota. For example, although production of PCBs in North America was banned in 1977, loadings of PCBs were higher than those of Polybrominated Diphenyl Ethers (PBDEs) from the city of Toronto to Lake Ontario in 2007 and 2008 (Melymuk et al. 2014). Although PCB production was restricted in 1974 onward to use in closed systems only, prior use in open use products such as caulking and sealants means that PCBs are still being released into the environment, thus maintaining their persistence. Assuming that the rate of degradation of POPs or loss in non-available compartments (e.g., buried in sediment, or transported outside of the Great Lakes through atmospheric transport) is exponential, not only is the temporal change in Herring Gulls likely to be exponential, but if the rates of decline of POPs slows in the Great Lakes, such changes are likely to be reflected within a similar timeframe in Herring Gull eggs.

There is little recent evidence that population numbers of colonial waterbirds in the Great Lakes are currently being limited by the direct effects of contaminants (Weseloh 2012), and productivity of Herring Gulls from colonies that once were reduced due to contaminants has returned to normal at many colonies in the Great Lakes. Nonetheless, contaminants may be having sublethal effects on gene expression or physiological responses of colonial waterbirds. Airborne polycyclic aromatic hydrocarbon exposure has been linked to the induction of mutations in Double-crested Cormorants (Phalacrocorax auritus; King et al. 2014) in Hamilton Harbour, and PBDEs have been associated with the suppression of transthyretin in neuronal cell lines of Herring Gulls (Crump et al. 2008). Recent evidence suggests that reduced prey availability may be contributing to population declines reported for colonial waterbirds such as Herring Gulls and Great Black-backed Gulls (L. marinus) nesting on the Great Lakes (Morris et al. 2003; Pekarik et al. 2016). By using ecological tracers, Hebert et al. (2008) found a temporal relationship between diet in Herring Gulls and a long-term decline in pelagic prey fish abundance. Concurrent with these changes, Hebert et al. (2009) found that egg volume of Herring Gulls also declined, putatively due to the reduction in fish prey availability. During periods of ecological stress, the effects of POPs may be exacerbated by worsened body conditions in Larids that are induced by limited food availability (Bustnes et al. 2008). Hence, the relationship among ecological changes, such as changes in food web structure or disease, may have complex interactions with contaminants in Great Lakes Herring Gulls.


Many people have assisted with the collection of Herring Gull eggs over the years and their efforts are greatly appreciated: Michael Gilbertson, Glen Fox, Andy Gilman, Doug Hallett, Jim Learning, John Elliott, Stan Teeple, Pierre Mineau, John Ryder, Gary Shugart, John Struger, Christine Bishop, Karen Pettit, Rob Dobos, Glenn Barrett, Cynthia Pekarik, Tania Havelka, Tammy Dobbie, Steve Elliott, Brian McHattie, Ralph Morris and his students, Jim Quinn and his students, Ray Faber and his students, Keith Grasman and his students, Lee Harper, Connie Adams, Susan Elbin, Liz Craig, Dave Best, Brian Ratcliff, Laird Shutt, Kim Williams, Doug Crump, Dave Ryckman, Margie Koster, Larry Benner, Earl Walker, Peter Ross, Tyler Hoar, Dave Andrews, Kate (Jermyn) Gee and Pete Ewins. Routine chemical analyses were directed by Richard Turle, Ross Norstrom, Bryan Wakeford and Abde Idrissi. Anonymous reviewers gave valuable comments.

Literature Cited


Ayris, S. and S. Harrad . 1999. The fate and persistence of polychlorinated biphenyls in soil. Journal of Environmental Monitoring 1: 395–401. Google Scholar


Bunnell, D. B. , R. P. Barbiero , S. A. Ludsin , C. P. Madenjian , G. J. Warren , D. M. Dolan , T. O. Brenden , R. Briland , O. T. Gorman , J. X. He and others. 2014. Changing ecosystem dynamics in the Laurentian Great Lakes: bottom-up and top-down regulation. BioScience 64: 26–39. Google Scholar


Bustnes, J. O. , P. Fauchald , T. Tveraa , M. Helberg and J. U. Skaare . 2008. The potential impact of environmental variation on the concentrations and ecological effects of pollutants in a marine avian top predator. Environment International 34: 193–201. Google Scholar


Crump, D. , S. Chiu , C. Egloff and S. W. Kennedy . 2008. Effects of hexabromocyclododecane and polybrominated diphenyl ethers on mRNA expression in chicken (Gallus domesticus) hepatocytes. Toxicological Sciences 106: 479–487. Google Scholar


de Solla, S. R. , D. V. C. Weseloh , R. J. Letcher and C. E. Hebert . 2010. Reconcilable differences: the use of reference material to reduce methodological artifacts in the reporting of organochlorine pesticides and polychlorinated biphenyls. Environmental Toxicology and Chemistry 29: 19–26. Google Scholar


Drouillard, K. G , I. Jezdic , S. M. O'Rourke , S. B. Gewurtz , A. A. Raeside , T. A. Leadley , P. Drca and G. D. Haffner . 2013. Spatial and temporal variability of PCBs in Detroit River water assessed using a long term biomonitoring program. Chemosphere 90: 95–102. Google Scholar


Fox, G. A. , A. P. Gilman , D. B. Peakall and F. W. Anderka . 1978. Behavioral abnormalities in nesting Lake Ontario Herring Gulls. Journal of Wildlife Management 42: 477–483. Google Scholar


Gandhi, N. , R. W. K. Tang , S. P. Bhavsar and G. B. Arhonditsis . 2014. Fish mercury levels appear to be increasing lately: a report from 40 years of monitoring in the province of Ontario, Canada. Environmental Science and Technology 48: 5404–5414. Google Scholar


Gauthier, L. T. , C. E. Hebert , D. V. C Weseloh and R. J. Letcher . 2007. Current-use flame retardants in the eggs of Herring Gulls (Larus argentatus) from the Laurentian Great Lakes. Environmental Science and Technology 41: 4561–4567. Google Scholar


Gauthier, L. T. , C. E. Hebert , D. V. C. Weseloh and R. J. Letcher . 2008. Dramatic changes in the temporal trends of polybrominated diphenyl ethers (PBDEs) in Herring Gull eggs from the Laurentian Great Lakes: 1982–2006. Environmental Science and Technology 42: 1524–1530. Google Scholar


Gewurtz, S. B. , S. P. Bhavsar , E. Awad , J. G. Winter , E. J. Reiner , R. Moody and R. Fletcher . 2011. Trends of legacy and emerging-issue contaminants in Lake Simcoe fishes. Journal of Great Lakes Research 37: 148–159. Google Scholar


Gilbertson, M. 1974. Seasonal changes in organochlorine compounds and mercury in Common Terns of Hamilton Harbour, Ontario. Bulletin of Environmental Contamination and Toxicology 12: 726–732. Google Scholar


Gilbertson, M. and L. M. Reynolds . 1972. Hexachlorobenzene (HCB) in the eggs of Common Terns in Hamilton Harbour, Ontario. Bulletin of Environmental Contamination and Toxicology 7: 371–373. Google Scholar


Gilbertson, M. and R. Hale . 1974. Early embryonic mortality in a Herring Gull colony in Lake Ontario. Canadian Field-Naturalist 88: 354–356. Google Scholar


Gilbertson, M. and G. A. Fox . 1977. Pollutant associated embryonic mortality of Great Lakes Herring Gulls. Environmental Pollution 12: 211–216. Google Scholar


Gilman, A. P. , G. A. Fox , D. B. Peakall , S. M. Teeple , T. R. Carroll and G. T. Haymes . 1977. Reproductive parameters and egg contaminant levels of Great Lakes Herring Gulls. Journal of Wildlife Management 41: 458–468. Google Scholar


Hebert, C. E. and D. V. C. Weseloh . 2006. Adjusting for temporal change in trophic position results in reduced rates of contaminant decline. Environmental Science and Technology 40: 5624–5628. Google Scholar


Hebert, C. E. , R. J. Norstrom and D. V. C. Weseloh . 1999. A quarter century of environmental surveillance: the Canadian Wildlife Service's Great Lakes Herring Gull monitoring program. Environmental Review 7: 147–166. Google Scholar


Hebert, C. E. , D. V. C. Weseloh , A. Idrissi , M. T. Arts and E. F. Roseman . 2009. Diets of aquatic birds reflect changes in the Lake Huron ecosystem. Aquatic Ecosystem Health and Management 12: 37–44. Google Scholar


Hebert, C. E. , R. J. Norstrom , M. Simon , B. M. Braune , D. V. C. Weseloh and C. R. Macdonald . 1994. Temporal trends and sources of PCDDs and PCDFs in the Great Lakes: Herring Gull egg monitoring 1981–1991. Environmental Science and Technology 28:1268–1277. Google Scholar


Hebert, C. E. , D. V. C. Weseloh , A. Idrissi , M. T. Arts , R. O'Gorman , O. T. Gorman , B. Locke , C. P. Madenjian and E. F. Roseman . 2008. Restoring piscivorous fish populations in the Laurentian Great Lakes causes seabird dietary change. Ecology 89: 891–897. Google Scholar


Hickey, J. P. , S. A. Batterman and S. M Chernyak . 2006. Trends of chlorinated organic contaminants in Great Lakes trout and Walleye from 1970 to 1998. Archives of Environmental Contamination and Toxicology 50: 97–110. Google Scholar


International Joint Commission (IJC). 1988. Revised Great Lakes Water Quality Agreement of 1978 as amended by Protocol signed November 18, 1987. Unpublished report, IJC United States and Canada, Washington, D.C. and Ottawa, Ontario. Google Scholar


Keith, J. A. 1966. Reproduction in a population of Herring Gulls (Larus argentatus) contaminated by DDT. Journal of Applied Ecology 3: 57–70. Google Scholar


King, L. E. , S. R. de Solla , J. M. Small , E. Sverko and J. S. Quinn . 2014. Microsatellite DNA mutations in Double-crested Cormorants (Phalacrocorax auritus) associated with exposure to PAH-containing industrial air pollution. Environmental Science and Technology 48: 11637–11645. Google Scholar


Letcher, R. J. , G. Su , J. N. Moore , L. L. Williams , P. A. Martin , S. R. de Solla and W. W. Bowman . 2015. Perfluorinated sulfonate and carboxylate compounds and their precursors in recent eggs of herring gulls from across the Laurentian Great Lakes of North America: distribution and exposure implications. Science of the Total Environment 538: 468–477. Google Scholar


Mackay, D. , S. Sang , P. Vlahos , M. L. Diamond , F. Gobas and D. Dolan . 1994. A rate constant model of chemical dynamics in a lake ecosystem: PCBs in Lake Ontario. Journal of Great Lakes Research 20: 625–642. Google Scholar


Melymuk, L. , M. Robson , S. A. Csiszar , P. A. Helm , G. Kaltenecker , S. Backus , L. Bradley , B. Gilbert , P. Blanchard , L. Jantunen and M. L. Diamond . 2014. From the city to the lake: loadings of PCBs, PBDEs, PAHs and PCMs from Toronto to Lake Ontario. Environmental Science and Technology 48: 3732–3741. Google Scholar


Morris, R. D. , D. V. Weseloh and J. L. Shutt . 2003. Distribution and abundance of nesting pairs of Herring Gulls (Larus argentatus) on the North American Great Lakes, 1976 to 2000. Journal of Great Lakes Research 29: 400–426. Google Scholar


Neff, M. R. , S. P. Bhavsar and J. X. Y. Chin . 2012. Spatial and temporal trends of muscle lipid content in Great Lakes fishes: 1970s-2008. Canadian Journal of Fisheries and Aquatic Sciences 69: 2007–2017. Google Scholar


Norstrom, R. J. and M. Simon . 1991. Determination of specific polychlorinated dibenzo-p-dioxins and dibenzofurans in biological matrices by gel-permeation-carbon chromatography and gas chromatography-mass spectrometry. Pages 281–297 in Environmental Carcinogens. Methods of Analysis and Exposure Measurement. Vol. II. Polychlorinated Dibenzodioxins and Dibenzofurans ( C. Rappe , H. R. Buser , B. Dodet and I. K. O'Neill , Eds.). World Health Organization, International Association for Research on Cancer, Lyon, France. Google Scholar


Norstrom, R. J. , H. T. Won , M. Van Hove Holdrinet , P. G. Calway and C. D. Naftel . 1980. Gas-liquid chromatographic determination of Mirex and photomirex in the presence of polychlorinated biphenyls: interlaboratory study. Journal of the Association of Official Analytical Chemists 63: 37–42. Google Scholar


Norstrom, R. J. , T. P. Clark , D. A. Jeffrey , H. T. Won and A. P. Gilman . 1986. Dynamics of organochlorine compounds in Herring Gulls (Larus argentatus): I. Distribution and clearance of [14C]DDE in free-living Herring Gulls (Larus argentatus). Environmental Toxicology and Chemistry 5: 41–48. Google Scholar


Norstrom, R. J. , M. Simon , J. Moisey , B. Wakeford and D. V. C. Weseloh . 2002. Geographic distribution (2000) and temporal trends (1981–2000) of brominated diphenyl ethers in Great Lakes Herring Gull eggs. Environmental Science and Technology 36: 4783–4789. Google Scholar


Payton, M. E. , M. H. Greenstone and N. Schenker . 2003. Overlapping confidence intervals or standard error intervals: what do they mean in terms of statistical significance? Journal of Insect Science 3: 34–40. Google Scholar


Pekarik, C. and D. V. Weseloh . 1998. Organochlorine contaminants in Herring Gull eggs from the Great Lakes, 1974–1995: change-point regression analysis and short-term regression. Environmental Monitoring and Assessment 53: 77–115. Google Scholar


Pekarik, C. , I. K. Barker and D. V. C. Weseloh . 2016. Organochlorine contaminants, immunocompetence and vitellogenin in Herring Gulls (Larus argentatus) and Great Black-backed Gulls (Larus marinus) nesting on Lake Ontario in 2001–2002. Waterbirds 39 (Special Publication 1): 180–201. Google Scholar


Reynolds, L. M. and T. Cooper . 1975. Analysis of organochlorine residues in fish. Water Quality Parameters, American Society for Testing and Materials - Standard Test Method 573: 196–205. Google Scholar


Rutkiewicz, J. , A. Scheuhammer , D. Crump , M. Jagla and N. Basu . 2010. Investigation of spatial trends and neurochemical impacts of mercury in Herring Gulls across the Laurentian Great Lakes. Environmental Pollution 158: 2733–2737. Google Scholar


Sadraddini, S. , M. E. Azim , Y. Shimoda , S. P. Bhavsar , K. G. Drouillard , S. M. Backus and G. B. Arhonditsis . 2011. A Bayesian assessment of the PCB temporal trends in Lake Erie fish communities. Journal of Great Lakes Research 37: 507–520. Google Scholar


Simon, M. and B. J. Wakeford . 2000. Multi-residue method for the determination of polychlorinated dibenzo-p-dioxins, polychlorinated dibenzofurans and non-ortho substituted polychlorinated biphenyls in wildlife tissues by HRGC/HRMS. Canadian Wildlife Service Technical Report Series No. 336. Canadian Wildlife Service, Headquarters, Hull, Québec. Google Scholar


Sinkkonen, S. and J. Paasivirta . 2000. Degradation halflife times of PCDDs, PCDFs and PCBs for environmental fate modeling. Chemosphere 40: 943–949. StatSoft, Inc. 2004. STATISTICA, v. 7. StatSoft, Inc., Tulsa, Oklahoma. Google Scholar


Su G. , R. J. Letcher , J. N. Moore , L. L. Williams , P. A. Martin , S. R. de Solla and W. W. Bowman . 2015. Spatial and temporal comparisons of legacy and emerging flame retardants in herring gull eggs from colonies spanning the Laurentian Great Lakes of Canada and United States. Environmental Research 142: 720–730. Google Scholar


Turle, R. and B. Collins . 1992. Validation of the use of pooled samples for monitoring of contaminants in wildlife. Chemosphere 25: 463–469. Google Scholar


Turle, R. , R. J. Norstrom and B. Collins . 1991. Comparison of PCB quantitation method: re-analysis of archived specimens of Herring Gull eggs from the Great Lakes. Chemosphere 22: 201–213. Google Scholar


Van Metre, P. C. , J. T. Wilson , E. Callender and C. C. Fuller . 1998. Similar rates of decrease of persistent, hydrophobic and particle-reactive contaminants in riverine systems. Environmental Science and Technology 32: 3312–3317. Google Scholar


Webster, E. , D. Mackay and K. Qiang . 1999. Equilibrium lipid partitioning concentrations as a multi-media synoptic indicator of contaminant levels and trends in aquatic ecosystems. Journal of Great Lakes Research 25: 318–329. Google Scholar


Weseloh, D. V. C. 2012. Contaminants in colonial waterbirds of the North American Great Lakes, 1955–2007. Pages 116–121 in Ecology and Animal Health, Ecosystem Health and Sustainable Agriculture 2 ( L. Norrgren and J. M. Levengood , Eds.). The Baltic University Programme, Uppsala University, Baltic University Press, Uppsala, Sweden. Google Scholar


Weseloh, D. V. , P. Mineau and J. Struger . 1990. Geographical distribution of contaminants and productivity measures of Herring Gulls in the Great Lakes: Lake Erie and connecting channels 1978/79. Science of the Total Environment 91: 141–159. Google Scholar


Weseloh, D. V. C. , R. A. Faber and C. Pekarik . 2005. Temporal and spatial trends of organochlorine contaminants in Herring Gull eggs from Lake Michigan. Pages 393–437 in State of Lake Michigan: Ecology, Health, and Management ( T. Edsall and M. Munawar , Eds.). Ecovision World Monograph Series, Aquatic Ecosystem Health and Management Society, Goodword Books Pvt. Ltd, New Delhi, India. Google Scholar


Weseloh, D. V. C. , C. Pekarik and S. R. de Solla . 2006. Spatial patterns and rankings of contaminant concentrations in Herring Gull eggs from 15 sites in the Great Lakes and connecting channels, 1988–2002. Environmental Monitoring and Assessment 113: 265–284. Google Scholar


Weseloh, D. V. , P. Hamr , C. A. Bishop and R. J. Norstrom . 1995. Organochlorine contaminant levels in waterbird species from Hamilton Harbour, Lake Ontario: an IJC area of concern. Journal of Great Lakes Research 21: 121–137. Google Scholar


Weseloh, D. V. , P. J. Ewins , J. Struger , P. Mineau and R. J. Norstrom . 1994. Geographical distribution of organochlorine contaminants and reproductive parameters in Herring Gulls on Lake Superior in 1983. Environmental Monitoring and Assessment 29: 229–251. Google Scholar


Weseloh, D. V. C. , D. J. Moore , C. E. Hebert , S. R. de Solla , B. M. Braune and D. McGoldrick . 2011. Current concentrations and spatial and temporal trends in mercury in Great Lakes Herring Gull eggs, 1974–2009. Ecotoxicology 20: 1644–1658. Google Scholar
Shane R. de Solla, D. V. Chip Weseloh, Kimberley D. Hughes, and David J. Moore "Forty-Year Decline of Organic Contaminants in Eggs of Herring Gulls (Larus argentatus) from the Great Lakes, 1974 to 2013," Waterbirds 39(sp1), 166-179, (1 April 2016).
Received: 2 June 2014; Accepted: 1 July 2015; Published: 1 April 2016

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