Retrospective Ecotoxicological Data and Current Information Needs for Terrestrial Vertebrates Residing in Coastal Habitat of the United States
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- Rattner, B.A., Eisenreich, K.M., Golden, N.H. et al. Arch Environ Contam Toxicol (2005) 49: 257. doi:10.1007/s00244-004-0193-y
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The Contaminant Exposure and Effects—Terrestrial Vertebrates (CEE-TV) database was developed to conduct simple searches for ecotoxicological information, examine exposure trends, and identify significant data gaps. The CEE-TV database contains 16,696 data records on free-ranging amphibians, reptiles, birds, and mammals residing in estuarine and coastal habitats of the Atlantic, Gulf, and Pacific coasts, Alaska, Hawaii, and the Great Lakes. Information in the database was derived from over 1800 source documents, representing 483 unique species (about 252,000 individuals), with sample collection dates spanning from 1884 to 2003. The majority of the records contain exposure data (generally contaminant concentrations) on a limited number (n = 209) of chlorinated and brominated compounds, cholinesterase-inhibiting pesticides, economic poisons, metals, and petroleum hydrocarbons, whereas only 9.3% of the records contain biomarker or bioindicator effects data. Temporal examination of exposure data provides evidence of declining concentrations of certain organochlorine pesticides in some avian species (e.g., ospreys, Pandion haliaetus), and an apparent increase in the detection and possibly the incidence of avian die-offs related to cholinesterase-inhibiting pesticides. To identify spatial data gaps, 11,360 database records with specific sampling locations were combined with the boundaries of coastal watersheds, and National Wildlife Refuge and National Park units. Terrestrial vertebrate ecotoxicological data were lacking in 41.9% of 464 coastal watersheds in the continental United States. Recent (1990–2003) terrestrial vertebrate contaminant exposure or effects data were available for only about half of the National Wildlife Refuge and National Park units in the geographic area encompassed by the database. When these data gaps were overlaid on watersheds exhibiting serious water quality problems and/or high vulnerability to pollution, 72 coastal watersheds, and 76 National Wildlife Refuge and 59 National Park units in the continental United States were found to lack recent terrestrial vertebrate ecotoxicology data. Delineation of data gaps in watersheds of concern can help prioritize monitoring in areas with impaired water quality and emphasize the need for comprehensive monitoring to gain a more complete understanding of coastal ecosystem health.
The Biomonitoring of Environmental Status and Trends (BEST) Program of the U.S. Geological Survey (USGS) (1) assesses the exposure and effects of environmental contaminants on select species and habitats throughout the United States, (2) conducts research and synthesis activities that provide biomonitoring methods for field application, and (3) supports the development of methods and tools to assist the U.S. Department of the Interior in assessing chemical threats to species and lands under its stewardship (Zylstra 1994; BEST 2003). Although there are many ecotoxicological monitoring programs that focus on aquatic species and habitats (Breckenridge et al.2003), the National Contaminant Biomonitoring Program (NCBP) of the U.S. Fish and Wildlife Service (US FWS) has been the only large-scale effort that has examined contaminant exposure in terrestrial vertebrates in the United States. The NCBP was discontinued in 1990 for a number of reasons (NRC 1995), including the decline in concentrations of organochlorine pesticides and total PCBs in mallard (Anas platyrhynchos) and black duck (A. rubripes) wings and European starling (Sturnus vulgaris) carcasses (Schmitt and Bunck 1995). However, organochlorine contaminants, metals, and new pollutants continue to pose hazards to terrestrial vertebrates at many geographic scales (i.e., small hazardous waste sites to entire watersheds). To address this hazard, the BEST Program seeks to identify critical data gaps through the retrospective compilation and analysis of ecotoxicological data, followed by active monitoring of terrestrial vertebrates at high priority sites and regions, as funding permits.
In 1996, efforts were initiated to develop and compile a “Contaminant Exposure and Effects–Terrestrial Vertebrates” (CEE-TV) database (Rattner et al.2000). Initially, work was focused on terrestrial vertebrates found in Atlantic estuarine habitats, but the geographic scope of the database has since been expanded to include estuarine and coastal habitat along the Gulf and Pacific coasts, Alaska, Hawaii, and the shoreline and islands on the Laurentian Great Lakes. The database became accessible in searchable format on the World Wide Web (http://www.pwrc.usgs. gov/contaminants-online) in 1999. The CEE-TV database has been used by many biologists and natural resource managers (Russom 2002) to conduct simple searches for exposure and biological effects information for a given species or location, identification of temporal contaminant exposure trends, data gap analyses for National Wildlife Refuge and National Park units, and ranking of terrestrial vertebrate ecotoxicological information needs based on data density and water quality problems. For example, there are no ecotoxicological data on terrestrial vertebrates from 1990 to 2000 (Cohen et al.2003) from 15 of the 136 Atlantic and Florida-Gulf coast watersheds classified by the U.S. Environmental Protection Agency (US EPA) Index of Watershed Indicators (IWI) (US EPA 1997a, 2000) as having water quality problems or high vulnerability to pollution. Furthermore, 59 of 132 (44.6%) National Wildlife Refuge and National Park units in watersheds of concern lack terrestrial vertebrate exposure and effects data for this same region and time period.
Herein we expand on our initial evaluation of the database (Rattner et al.2000), with special emphasis on spatial and temporal data gaps in measures of contaminant exposure for terrestrial vertebrates residing in the Atlantic, Gulf, and Pacific coasts, Alaska, Hawaii, and the Great Lakes. Our intent is to provide scientists and natural resource managers essential information that will aid in the prioritization of contaminant biomonitoring in watersheds, and units of the National Wildlife Refuge System and National Park System.
Materials and Methods
Data Acquisition and Database Design
Retrospective contaminant exposure and effects data for free-ranging terrestrial vertebrates residing in U.S. estuarine and coastal habitat were identified and compiled using scientific literature search tools (e.g., Wildlife Review, BIOSIS, TOXLINE, AGRICOLA), by examining various databases (e.g., US EPA Ecological Incident Information System, US FWS Environmental Contaminant Data Management System, USGS National Wildlife Health Center Mortality Database), and through communication with 480 scientists in federal and state agencies, conservation organizations, and academic institutions. Source documents were reviewed to identify data collected in estuarine and coastal drainages, and, unless obvious flaws in data quality were apparent, information was coded for database entry. All data were referenced with geographic collection coordinates, and if absent from the source document, coordinates were assigned based on the location description using MapExpert version 2.0 (DeLorme Mapping, Freeport, ME, USA), USGS Geographic Names Information System (http://geonames.usgs.gov/gnishome.html), or the Canadian Geographical Names website (http://geonames.nrcan.gc.ca/index_e.php). If samples were collected across an entire county, the coordinates of the county seat were assigned to the record. If the samples were collected across an entire state or the collection location in the state was not specified, the coordinates of the state capital were assigned to the record. Data were compiled in a 118-field database in Microsoft Access 2000 version 9.0 (Microsoft Corp., Redmond, WA, USA) with information describing taxonomy, collection date, study location, geographic coordinates, sample matrix, contaminant concentration, biomarker or bioindicator response, and source of information. Additional details of the CEE-TV database have been published (Rattner et al.2000) and are available on the Internet (http://www.pwrc.usgs.gov/contaminants-online).
Descriptive and Geographic Analyses
The CEE-TV database was sorted and queried for phylogenetic, temporal, spatial, and contaminant exposure and response patterns using search features of Access. Maps of record locations were created using ArcGIS 8.2 (Environmental Systems Research Institute, Inc., Redlands, CA 2000) geographic information systems software, and overlaid on boundary maps of watersheds (defined by USGS 8-digit Hydrologic Unit Codes), and National Wildlife Refuge and National Park units.
Spatial information gap analyses were conducted by overlaying locations of CEE-TV records on these maps. To avoid the potential bias of records with coordinates assigned to a county seat or state capital, only records with known collection coordinates were used in geospatial analyses. Data gaps were defined as recent if there are no records with data collected from 1990 to 2003; data gaps were defined as historic if there are no records with data prior to 1990. To account for possible imprecision and uncertainty of sampling coordinates, maps with a 1-km buffer were created around each National Wildlife Refuge and National Park property boundary, and to account for animal movement, 10-km buffers were used around each of these management units.
In order to identify the information data gaps that are of greatest concern, the buffered National Wildlife Refuge and National Park units were overlaid on the IWI (US EPA 1997a, 2000). The IWI classifies watershed water quality from “better” to “more serious” as well as watershed vulnerability (i.e., potential for discharges and other stressors to affect water quality) from “low” to “high.” The IWI rankings were joined by Hydrologic Unit Codes to the watershed database, creating a map identifying watersheds of concern (i.e., IWI classifications of more serious water quality problems and/or high vulnerability to pollution). Each of the management units that intersected watersheds of concern was placed into a separate map for further information gap analysis.
Results and Discussion
Source Documents and Composition of the CEE-TV Database
As of December 2003, the CEE-TV database contained a total of 16,696 records. Many of the reference sources contained data from multiple sample matrices collected from numerous sampling locations, and more than one species; thus a single source document frequently generated many geo-referenced records. The 1849 source documents used for this database included 718 published journal articles, 63 peer-reviewed conference proceedings or books, 11 abstracts from scientific meetings, 20 Master’s thesis or Doctoral dissertation documents, 854 necropsy reports, 167 reports or unpublished manuscripts, and 16 records from other databases.
The number of organisms per record ranged from 1 to 37,590, with about 50% of the records containing information on multiple individuals. Because several sample matrices were often quantified in a single organism, and occasionally pooled tissue samples were analyzed, the total number of unique individuals in the database is estimated to be 252,000. Fifty-five different sample matrices were quantified, with the most common matrix being egg content, followed, in decreasing order, by liver, brain, carcass, muscle, kidney, adipose, blood, wing, feather, eggshell, gizzard, gastrointestinal tract, and hair.
The geographic coordinates of 5336 records (31.9% of the total) were not precisely described in source documents, and were thus assigned to the corresponding county seat or state capital. This deficiency often reflects (1) the type of investigation (e.g., necropsy report that identifies collection site only to the county level, regional waterfowl flyway surveys that are summarized by state), (2) the time-consuming nature of determining exact collection sites prior to the advent of handheld GPS units, and in rare instances, (3) hesitancy to report sampling location because of ongoing litigation or the threatened or endangered status of the species being studied.
The CEE-TV database is updated on an annual basis. The sample collection date ranges from 1884 to 2003. For the 16,360 records for which the sample collection date was specified, the distribution of records among decades is 9.9% for the 1960s, 30.2% for the 1970s, 31.0% for the 1980s, and 23.3% for the 1990s. These findings are in contrast to our earlier report (Rattner et al.2000) that suggested that sampling of terrestrial vertebrates for ecotoxicological exposure or effects endpoints along the Atlantic and Florida Gulf coast had declined even more markedly since the 1970s.
Phylogenetic distribution of records in the Contaminant Exposure and Effects — Terrestrial Vertebrates (CEE-TV) database
Artiodactyla (even-toed ungulates)
Carnivora (true carnivores)
Didelphimorphia (New World opossums)
Insectivora (shrews and moles)
Lagomorpha (pikas, rabbits and hares)
Charadriiformes (shorebirds, gulls, and allies)
Ciconiiformes (herons, storks, and allies)
Columbiformes (pigeons and doves)
Falconiformes (diurnal birds of prey)
Gruiformes (cranes, rails, and allies)
Passeriformes (song birds)
Pelecaniformes (pelicans and allies)
Piciformes (woodpeckers and allies)
Procellariiformes (albatross, petrels, and allies)
Anura (frogs and toads)
Contaminant Exposure and Effect Endpoints
Frequency of various measurement endpoints in the Contaminant Exposure and Effects—Terrestrial Vertebrates (CEE-TV) database
Exposure and effect endpoint
Number of CEE-TV records with endpoint examined
Number of CEE-TV records with detectable concentrations
Organochorine pesticides and metabolites
p,p′-DDD; p,p′-DDE; p,p′- DDT
Other organochlorine contaminants
Total PCBs (aroclors)
Dioxins and dibenzofurans
Metals, metalloids and trace elements
Shot used in hunting
Biomarker/bioindicator effect responses
Aminolevulinic acid dehydratase activity
Oxidative stress endpoints
Information on biological effects potentially related to contaminant exposure occurs in 9.3% of the records in the database. The most frequently measured effect endpoint is eggshell thinning associated with exposure to p,p′-DDE or other organochlorine pesticides, although the majority of the effect measurements conducted since 1980 involved biochemical biomarkers (e.g., cholinesterase, cytochrome P450, DNA damage, measures of oxidative stress, and protoporphyrin).
A number of interesting exposure and effects trends are apparent upon examination of the CEE-TV database. For example, in a retrospective evaluation (1965–1994) of contaminants in osprey (Pandion haliaetus) eggs for the Atlantic coast (Rattner et al.2000), we reported that p,p′-DDE concentrations had declined since the 1970s, presumably reflecting restrictions imposed on its use and its degradation in the environment over time. A reanalysis with an expanded dataset for the Atlantic coast from 1965 to 2003 further documented this decline (p < 0.05; sample size weighted analysis of variance of log transformed data and Student-Newman-Keuls multiple range test): 1965–1974, geometric mean p,p′-DDE = 3.97 μg/g wet weight, n = 38 records representing 191 eggs; 1975–1984, 2.90 μg/g, n = 17 records representing 98 eggs; 1985–1994, 1.50 μg/g, n = 9 records representing 47 eggs; 1995–2003, 0.62 μg/g, n = 8 records representing 92 eggs. Despite a seemingly downward trend, total PCBs in these same samples did not decline significantly (p > 0.25) over time (1965–1974, geometric mean total PCBs = 5.18 μg/g wet weight; 1975–1984, 6.87 μg/g; 1985–1994, 4.11 μg/g; 1995–2003, 4.70 μg/g).
Organophosphorus and carbamate pesticide exposure information (i.e., residues in tissue or digestive tract and/or ≥ 20% inhibition of brain cholinesterase activity; n = 302 records) in the CEE-TV database was compared with a retrospective analysis of confirmed and suspected anticholinesterase (antiChE) poisoning events (n = 335) (Fleischli et al.2004) from the National Wildlife Health Center (NWHC) mortality database. There are considerable differences in the scope of these two databases, including diverse information sources in CEE-TV versus analysis of submitted specimens in NWHC mortality database, estuarine and coastal drainages in 30 states, and the District of Columbia versus entire United States, and incidents from 1963 to 2003 versus incidents from 1980 to 2000. Therefore, it is not surprising that only 24 records in the CEE-TV database are in the NWHC mortality database. Anticholinesterase pesticide exposure data in the CEE-TV database include 58 species of birds and 2 mammals, compared to 103 avian species in the NWHC mortality database. The rank order of antiChE pesticide exposure in the CEE-TV database was Passeriformes (n = 153 records) > Anseriformes (n = 77) > Charadriiformes (n = 29) > Falconiformes (n = 22), whereas the rank order in the NWHC mortality database was Falconiformes (n = 165) > Anseriformes (n = 112) > Passeriformes (n = 79) > Columbiformes (n = 18). The differences are probably due, at least in part, to differences in the geographic scope of these databases. Diazinon, carbofuran, parathion, and monocrotophos were the most common antiChE pesticides in the CEE-TV database, whereas famphur, carbofuran, diazinon, and fenthion were most prevalent in the NWHC mortality database. Anticholinesterase pesticide exposure records in the CEE-TV database have increased steadily over time (before 1970, 2 records; 1970–1979, 28 records; 1980–1989, 52 records; 1990–2003, 220 records), presumably reflecting both increased use of these pesticides, and also perhaps more efficient detection and reporting of exposure and die-off events.
Of 3600 records containing information on mercury exposure, only 6 included information regarding adverse effects (i.e., possible mercury poisoning). More than half of all mercury records contained information for fish-eating birds (n = 1942), with the herring gull (n = 339), common loon (Gavia immer, n = 214), and bald eagle (Haliaeetus leucocephalus, n = 196) accounting for more data than any other individual species. No temporal trends were found for mercury in eggs of fish-eating birds, although regional differences were apparent. For the continental United States, the geometric mean concentration in eggs collected from the Atlantic Coast (0.39 μg/g wet weight, n = 141 records representing 986 eggs) was higher (p < 0.05; sample size weighted analysis of variance of log transformed data and Student-Newman-Keuls multiple range test) than concentrations in eggs collected from the Pacific Coast (0.29 μg/g, n = 39 records representing 451 eggs) and Gulf Coast (0.24 μg/g, n = 65 records representing 309 eggs), but did not differ from that of the Great Lakes (0.32 μg/g, n = 431 records representing 3421 eggs). This trend is generally consistent with both the US EPA’s reporting of higher mercury emissions in the eastern United States and recent findings of increasing blood mercury concentrations in loons as collection sites ranged from west to east (US EPA 1997b; Evers et al. 1998). For fish-eating birds in Florida, mean mercury concentrations in eggs (0.18 μg/g) were lower than regional averages, after the removal of one atypically high data point (7.93 μg/g in 12 sooty tern, Sternafuscata, eggs from the Dry Tortugas). However, mercury concentrations in feathers, at or exceeding levels associated with adverse effects (5 μg/g dry weight; Eisler 2000), were found in a greater percentage of birds in Florida (50%, n = 35 of 71 records) than all other states combined (15%, n = 13 of 88 records).
Estuarine and coastal drainages of the continental United States lacking recent (1990–2003) Contaminant Exposure and Effects— Terrestrial Vertebrates (CEE-TV) data
Hydrologic unit code
Largest watersheds or portion of watersheds lacking recent data
Northwestern Lake Superior
Eastern Lower Delmarva
Watersheds with “more serious water quality problems” and “high vulnerability to pollution” lacking recent data
Middle Delaware River
Western Mississippi Sound
Central San Francisco/San Pablo/Suisin Bays
Central San Francisco/San Pablo/Suisun Bays
National Wildlife Refuge and National Park units in coastal and estuarine drainages of the continental United States lacking recent (1990–2003) Contaminant Exposure and Effects—Terrestrial Vertebrates (CEE-TV) data
Management unit name
Refuge and park unitarea including buffer (km2)
Largest National Wildlife Refuge (NWR) units lacking dataa
Lower Suwannee NWR
Bon Secour NWR
Hobe Sound NWR
Big Branch Marsh NWR
Grand Bay NWR
Largest National Park units lacking dataa
Sleeping Bear Dunes National Lakeshore
Petersburg National Battlefield
Minute Man National Historic Park
Grand Portage National Monument
George Washington Birthplace National Monument
Fort Matanzas National Monument
Cuyahoga Valley National Park
Canaveral National Seashore
Biscayne National Park
Big Thicket National Preserve
Units in watersheds with “more serious water quality problems” and “high vulnerability to pollution” lacking datab
Bayou Teche NWR
Minute Man National Historic Park
John Muir National Historic Site
Presidio National Park
Muir Woods National Monument
Boston National Historic Park
Statue of Liberty National Monument
Boston African-American National Historic Site
Edison National Historic Site
It is recognized that these analyses have potential sources of bias and inaccuracy. For example, although most of the published data were acquired, undoubtedly not all of the unpublished data were obtained. Some collection locations were either not reported in the literature or locations were inaccurate, making it difficult to evaluate individual sites. Finally, although most documents were peer reviewed, there are always concerns about comparability of analytical results. Nonetheless, the findings of our analyses reveal some trends that deserve attention. Despite widespread concerns about environmental pollution, we found that during the past decade only about one-half of the coastal National Wildlife Refuge and National Park units appear to have terrestrial vertebrate ecotoxicological data. In addition, a significant number of these units (76 National Wildlife Refuge and 59 National Park units representing about 20,000 km2) fall within watersheds of concern. Based upon known water quality problems and vulnerability to pollution, we identified a preliminary list of U.S. Department of the Interior management units where terrestrial vertebrate ecotoxicology monitoring appears to be most warranted. In order to best assess large-scale terrestrial vertebrate ecotoxicological trends in the United States, a monitoring program that incorporates some form of random sampling is warranted, in addition to spatial and temporal replication. At a minimum, a regionalized program or efforts focused on lands in watersheds of concern might help detect effects in localized areas and prevent serious natural resource problems.
We thank Lynda J. Garret, Wanda Manning, and Kathryn A. Mannstedt for assistance with the computerized literature searches and data retrieval; Craig R. Beckman, Eileen K. Henniger, Rebecca L. Kershnar, Elise A. Larsen, Katie L. Lobner, Anne M. Meckstroth, and Craig W. Meeusen for compiling and coding database records; and Jonathan B. Cohen and James J. Coyle for reviewing a draft of this manuscript.