Utilizing the Great Blue Heron (Ardea Herodias) in Ecological Risk Assessments of Bioaccumulative Contaminants
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Environ Monit Assess (2009) 157:199–210 DOI 10.1007/s10661-008-0528-7 Utilizing the great blue heron (Ardea herodias) in ecological risk assessments of bioaccumulative contaminants Rita Marie Seston · Matthew John Zwiernik · Timothy Brian Fredricks · Sarah Jean Coefield · Dustin Lee Tazelaar · David Wayne Hamman · John David Paulson · John Paul Giesy Received: 10 February 2008 / Accepted: 11 September 2008 / Published online: 11 October 2008 © The Author(s) 2008. This article is published with open access at Springerlink.com Abstract Selection of an appropriate species is ease of study, high potential for exposure, wide- a key element of effective ecological risk assess- spread distribution, and territorial foraging be- ments (ERA), especially when site-specific field havior. Methodologies for assessing exposure and studies are to be employed. Great blue herons population health are described herein. As out- (GBH) possess several ideal characteristics of a lined, the collection of GBH eggs, GBH nestling receptor species for the assessment of bioaccu- blood, and adult GBH blood allows for the de- mulative compounds in the environment, such as termination of contaminant concentrations in var- ious GBH tissues, a top-down assessment, which can be done in conjunction with predicted dietary R. M. Seston (B) · M. J. Zwiernik · T. B. Fredricks · exposure, a bottom-up assessment, to support a S. J. Coefield · D. L. Tazelaar · J. P. Giesy multiple lines of evidence approach. Additionally, Zoology Department, Center for Integrative population parameters, such as productivity and Toxicology, National Food Safety and Toxicology survival, can also be measured to elucidate if the Center, Michigan State University, East Lansing, MI 48824, USA contaminant exposure may be causing population e-mail: [email protected] level effects. Over the course of two years, three GBH rookeries were monitored for productivity D. W. Hamman and nestling exposure. Nests were monitored from College of Veterinary Medicine, Center for Comparative Epidemiology, blinds and individually accessed at multiple time Michigan State University, East Lansing, points to obtain measures of nestling health, band MI 48824, USA nestlings, and collect eggs and nestling plasma. Multiple nests could frequently be accessed by J. D. Paulson Wildlife Services, USDA-APHIS, Bismarck, climbing one tree, resulting in minimal effort to ND 58501, USA obtain the necessary sample size. Additionally, 51 adult GBH, captured in their foraging areas, were J. P. Giesy banded, and provided a blood sample. With these Department of Veterinary Biomedical Sciences and Toxicology Centre, University of Saskatchewan, samples, a statistical difference in tissue based Saskatoon, Saskatchewan S7J 5B3, Canada exposure was identified between the reference and target area. Statistically significant differences J. P. Giesy were also identified between the upper and lower Department of Biology and Chemistry, City University of Hong Kong, Kowloon, reaches of the target area, thereby identifying Hong Kong SAR, China a range of doses geographically which could be 200 Environ Monit Assess (2009) 157:199–210 correlated to specific measurement endpoints. upstream boundary of the study area is a low-head The ability to identify a dose response greatly dam. Throughout the study area, the river is free increases the ability of the dataset to determine flowing to the confluence with the Saginaw River causation, a key goal of such studies. Overall, and eventually Saginaw Bay and Lake Huron. The the use of the described methods allowed for the study area was selected because soils and sedi- collection of a statistically sufficient and ecologi- ments were found to contain elevated concentra- cally relevant dataset with reasonable effort and tions of PCDFs and PCDDs. Soils and sediments minimal impact on GBH. collected from within the study area contained mean PCDF/PCDD concentrations ranging from Keywords Avian · Bird · Egg · PCDD · PCDF · 1.0 × 102 to 5.4 × 104 pg/g dw, which were ten- Plasma · Tittabawassee · Trapping to 20-fold greater than those collected upstream in reference areas (Hilscherova et al. 2003). The source of this contamination has been identified Introduction as The Dow Chemical Company (USEPA 1986). PCDFs and PCDDs occur in the environment Selection of appropriate species is a key ele- as mixtures and due to their hydrophobic charac- ment to allow effective ecological risk assessments teristics and resistance toward metabolism, they (ERA), especially when site-specific field stud- have great potential to be accumulated through ies are to be employed. Ideally, representative the food web. The toxicological response of pri- species used in assessments of bioaccumulative mary concern is mediated through the aryl hy- compounds should have an elevated exposure po- drocarbon receptor (AhR) and effects include tential, a widespread distribution, and be terri- carcinogenicity, immunotoxicity, and adverse ef- torial. Data collected using the selected species fects on reproduction, development, and en- should ultimately provide insight into the health docrine functions (van den Berg et al. 1998). In of the entire ecosystem of the study site. Piscivo- particular, AhR-mediated compounds have been rous birds are frequently selected as receptors for shown to decrease hatching success and fledging evaluating aquatic systems because they can be success in aquatic avian species (Gilbertson 1983; sensitive to the effects of contaminants and have Hoffman et al. 1987; Ludwig et al. 1993; van den the potential to accumulate persistent, lipophylic Berg et al. 1994). contaminants through trophic-transfer. The great Desirable, species-specific characteristics of the blue heron (Ardea herodias; GBH) possesses sev- GBH led to its inclusion as a receptor species in eral characteristics that make it an appropriate an ERA concerning PCDFs and PCDDs along the species to use as a receptor in ERAs concerning Tittabawassee River and its floodplain. The objec- bioaccumulative contaminants in aquatic environ- tive of this paper is to outline a series of methods ments. Here we describe a multiple lines of evi- and the associated effort necessary to effectively dence approach to elucidating exposure of GBH employ the GBH as a receptor in an ERA utilizing to contaminants through the diet and measured a multiple line of evidence approach. concentrations in specific GBH tissues. As a case study of the methodology, we have investigated the exposure of GBH to polychlorinated dibenzo- Species applicability furans (PCDFs) and dibenzo-p-dioxins (PCDDs) in the Tittabawassee River basin, Michigan, USA. Species-specific attributes need to be considered The Tittabawassee River study area includes when selecting a species for use as a receptor. approximately 37 km of the Tittabawassee River GBH possess many of the characteristics that from the upstream boundary of the city lim- are desirable in a receptor species, and as such, its of Midland, MI to the confluence of the are often selected as an ecological receptor of Tittabawassee and Saginaw Rivers downstream concern in risk assessments. GBH have a broad of Green Point Island (Fig. 1). Just above the distribution across geographic regions and habitat Environ Monit Assess (2009) 157:199–210 201 Fig. 1 Location of great blue heron rookeries (FRE, SNWR, and CAS) and reaches within the Tittabawassee River study area, MI, USA where trapping occurred types, residing in freshwater, estuarine, and ma- As a long-lived territorial species at the top of rine habitats throughout North America (Butler the aquatic food web, GBH have the potential 1992). GBH are a colonially-nesting species, with to bioaccumulate local contaminants over a long a rookery containing as many as 1,300 breed- period of time (Custer et al. 1991). Band recov- ing pairs recorded (DesGranges and Desrosiers eries have shown GBH may live to be at least 2006). With breeding pairs concentrated in one 20 years old (Bayer 1981). GBH are year-round area, the colonies are more conspicuous to re- residents in areas of its range where foraging searchers than single-nesting species which allows remains available during winter months, particu- for the assessment of population health rather larly in coastal areas (Butler 1997). The territorial than the outcome of a few nesting pairs. There nature of GBH leads to the active defense of are many closely related species for which GBH distinct, identifiable foraging areas local to the could serve as a surrogate species or that could breeding colony (Peifer 1979;Marion1989), thus be studied utilizing the described methods. Ad- GBH exposure may have a greater spatial resolu- ditionally, GBH are a charismatic species that is tion as compared to other more opportunistically widely recognized by the general public, which feeding piscivorous birds. Previous studies have would have an interest in preserving this species. detected local organochlorine contaminants in the 202 Environ Monit Assess (2009) 157:199–210 tissues of GBH (Custer et al. 1997; Thomas and the trees to make a count of the total number of Anthony 1999; Elliott et al. 2001; Champoux et al. nests. 2002; Harris et al. 2003;Straubetal.2007). Nests were located in Eastern cottonwood (Populus deltoides), silver maple (Acer sacchar- inum), or white ash (Fraxinus americana) trees at heights ranging between 15 and 25 m. Viable Methods and nonviable eggs were collected from accessi- ble nests in each nesting colony. Nest trees were Nest monitoring and fresh egg sampling selected