Robert A. Grove

Nineteenth Century Mercury: Hazard to Wading Birds and Cormorants of the Carson River, Nevada

Contemporary mercury interest relates to atmospheric deposition, contaminated fish stocks and exposed fish-eating wildlife. The focus is on methylmercury (MeHg) even though most contamination is of inorganic (IoHg) origin. However, IoHg is readily methylated in aquatic systems to become more hazardous to vertebrates. In response to a classic episode of historical (1859–1890) IoHg contamination, we studied fish-eating birds nesting along the lower Carson River, Nevada. Adult double-crested cormorants (Phalacrocorax auritus), snowy egrets (Egretta thula) and black-crowned night-herons (Nycticorax nycticorax) contained very high concentrations of total mercury (THg) in their livers (geo. means 134.8μg/g wet weight (ww), 43.7 and 13.5, respectively) and kidneys (69.4, 11.1 and 6.1, respectively). Apparently tolerance of these concentrations was possible due to a threshold-dependent demethylation coupled with sequestration of resultant IoHg. Demethylation and sequestration processes also appeared to have reduced the amount of MeHg redistributed to eggs. However, the relatively short time spent by adults in the contaminated area before egg laying was also a factor in lower than expected concentrations of mercury in eggs. Most eggs (100% MeHg) had concentrations below 0.80μg/g ww, the putative threshold concentration where reproductive problems may be expected; there was no conclusive evidence of mercury-related depressed hatchability. After hatching, the young birds were fed diets by their parents averaging 0.36–1.18μgMeHg/g ww through fledging. During this four to six week period, accumulated mercury concentrations in the organs of the fledglings were much lower than found in adults, but evidence was detected of toxicity to their immune (spleen, thymus, bursa), detoxicating (liver, kidneys) and nervous systems. Several indications of oxidative stress were also noted in the fledglings and were most apparent in young cormorants containing highest concentrations of mercury. This stress was evidenced by increased thiobarbituric acid-reactive substances, low activities of enzymes related to glutathione metabolism and low levels of reduced thiols, plus an increase in the ratio of oxidized to reduced glutathione. At lower concentrations of mercury, as was found in young egrets, we observed elevated activities of protective hepatic enzymes, which could help reduce oxidative stress. Immune deficiencies and neurological impairment of fledglings may affect survivability when confronted with the stresses of learning to forage and the ability to complete their first migration.

Osprey: Worldwide Sentinel Species for Assessing and Monitoring Environmental Contamination in Rivers, Lakes, Reservoirs, and Estuaries

In the United States, many fish and wildlife species have been used nationwide to monitor environmental contaminant exposure and effects, including carcasses of the bald eagle (Haliaeetus leucocephalus), the only top avian predator regularly used in the past. Unfortunately, bald eagles are sensitive to investigator intrusion at the nest. Thus, the osprey (Pandion haliaetus) is evaluated as a potential sentinel species for aquatic ecosystems. Several characteristics support the choice of the osprey as a sentinel species, including: (1) fish-eating diet atop the aquatic food web, (2) long-lived with strong nest fidelity, (3) adapts to human landscapes (potentially the most contaminated), (4) tolerates short-term nest disturbance, (5) nests spatially distributed at regular intervals, (6) highly visible nests easily located for study, (7) ability to accumulate most, if not all, lipophilic contaminants, (8) known sensitivity to many contaminants, and (9) nearly a worldwide distribution. These osprey traits have been instrumental in successfully using the species to understand population distribution, abundance, and changes over time; the effects of various contaminants on reproductive success; how contaminants in prey (fish on biomass basis) contribute to egg concentrations (i.e., biomagnification factors); and spatial residue patterns. Data summarized include nesting population surveys, detailed nesting studies, and chemical analyses of osprey egg, organ, blood, and feather samples for contaminants that bioaccumulate and/or biomagnify in aquatic food webs; and biochemical evaluations of blood and various organs. Studies in the United States, Canada, Mexico, Europe, and elsewhere have shown the osprey to be a useful sentinel species for monitoring selected environmental contaminants, including some emerging contaminants in lakes, reservoirs, rivers, and estuaries.

Biomagnification factors (fish to Osprey eggs from Willamette River, Oregon, U.S.A.) for PCDDs, PCDFs, PCBs and OC pesticides.

A migratory population of 78 pairs of Osprey (Pandion haliaetus) nesting along the Willamette River in westernOregon was studied in 1993. The study was designed to determinecontaminant concentrations in eggs, contaminant concentrationsin fish species predominant in the Ospreys diet, andBiomagnification Factors (BMFs) of contaminants from fish specieseaten to Osprey eggs. Ten Osprey eggs and 25 composite samplesof fish (3 species) were used to evaluate organochlorine (OC)pesticides, polychlorinated biphenyls (PCBs), polychlorinateddibenzo-p-dioxins (PCDDs), and polychlorinated dibenzofurans(PCDFs). Mercury was also analyzed in fish. Geometric meanresidues in Osprey eggs were judged low, e.g., DDE 2.3 μg g-1 wet weight (ww), Σ PCBs 0.69 μg g-1, 2,3,7,8-TCDD 2.3 ng kg-1, and generally well below known threshold values for adverse effects on productivity, and the population was increasing. Osprey egg residue data presentedby River Mile (RM) are discussed, e.g., higher PCDDs were generally found immediately downstream of paper mills and eggsfrom the Willamette River had significantly elevated PCBs and PCDDs compared to reference eggs collected nearby in the CascadeMountains. Prey remains at nest sites indicated that the Largescale Sucker (Catostomus macrocheilus) and NorthernPikeminnow (Ptychocheilus oregonensis) accounted for an estimated 90.1% of the biomass in the Osprey diet, and composite samples of these two species were collected from different sampling sites throughout the study area for contaminant analyses. With the large percentage of the fishbiomass in the Osprey diet sampled for contaminants (and fisheaten by Ospreys similar in size to those chemically analyzed),and fish contaminant concentrations weighted by biomass intake, a mean BMF was estimated from fish to Osprey eggs for the largeseries of contaminants. BMFs ranged from no biomagnification(0.42) for 2,3,7,8-TCDF to 174 for OCDD. Our findings for themigratory Osprey were compared to BMFs for the resident HerringGull (Larus argentatus), and differences are discussed. Webelieve a BMF approach provides some basic understanding ofrelationships between contaminant burdens in prey species offish-eating birds and contaminants incorporated into their eggs,and may prove useful in understanding sources of contaminants inmigratory species although additional studies are needed.

Accumulation of trace elements and organochlorines by surf scoters wintering in the Pacific northwest

ABSTRACr-Selenium, cadmium, mercury, copper, manganese, zinc, aluminum, lead, PCBs and DDE were accumulated by segments of the surf scoter (Melanitta perspicillata) population that winters in the Pacific Northwest, but whether the uptake occurred on breeding and/or wintering grounds was uncertain for some contaminants. Surf scoters collected in Puget Sound and San Francisco Bay (in another study) during the same period (January 1985) contained similar concentrations of cadmium, but Alsea Bay scoters contained more. Cadmium was inversely related to both liver and body weights of Northwest scoters in January; similar weight losses were reported in experimental laboratory studies. Northwest and north San Francisco Bay scoters contained similar mercury concentrations, but those in south San Francisco Bay contained higher concentrations. San Francisco Bay scoters contained higher arsenic and selenium concentrations than those in the Northwest; however, the 43.4 ppm (geometric mean, dry wt) selenium in livers at Commencement Bay in January was above levels associated with the reproductive problems in aquatic birds at Kesterson National Wildlife Refuge. Even higher concentrations of some elements may be found in surf scoters in March, because a later collection (March) at San Francisco Bay yielded higher concentrations than found there in January. Trace element concentrations in birds at a given wintering location are variable among species and may be influenced by diet, breeding grounds, and physiology (e.g., at Commencement Bay surf scoters with a sediment-associated diet contained 50X more cadmium in their kidneys than did fish-eating western grebes [Aechmophorus occidentalis]). The numerous wildlife species that live on estuaries require further attention.

Contaminants of legacy and emerging concern in largescale suckers (Catostomus macrocheilus) and the foodweb in the lower Columbia River, Oregon and Washington, USA

We investigated occurrence, transport pathways, and effects of polybrominated diphenyl ether (PBDE) flame retardants and other endocrine disrupting chemicals (EDCs) in aquatic media and the foodweb in the lower Columbia River. In 2009 and 2010, foodweb sampling at three sites along a gradient of contaminant exposure near Skamania (Washington), Columbia City (Oregon) and Longview (Washington) included water (via passive samplers), bed sediment, invertebrate biomass residing in sediment, a resident fish species (largescale suckers [Catostomus macrocheilus]), and eggs from osprey (Pandion haliaetus). This paper primarily reports fish tissue concentrations. In 2009, composites of fish brain, fillet, liver, stomach, and gonad tissues revealed that overall contaminant concentrations were highest in livers, followed by brain, stomach, gonad, and fillet. Concentrations of halogenated compounds in tissue samples from all three sites ranged from <1 to 400nanograms per gram of wet tissue. Several chemical classes, including PBDEs, organochlorine pesticides, and polychlorinated biphenyls (PCBs), were detected at all sites and in nearly all fish tissues sampled. In 2010, only fish livers were sampled and inter-site concentration differences were not as pronounced as in 2009. Chemical concentrations in sediments, fish tissues, and osprey eggs increased moving downstream from Skamania to the urbanized sites near Columbia City and Longview. Numerous organochlorine (OC) pesticides, both banned and currently used, and PBDEs, were present at each site in multiple media and concentrations exceeded environmental quality benchmarks in some cases. Frequently detected OC compounds included hexachlorobenzene, pentachloroanisole, dichlorodiphenyltrichloroethane (DDT) and its degradates, chlorpyrifos, and oxyfluorofen. Biomagnification of BDE47, 100, 153, and 154 occurred in largescale suckers and osprey eggs. Results support the hypothesis that contaminants in the environment lead to bioaccumulation and potential negative effects in multiple levels of the foodweb.

Mercury and Drought Along the Lower Carson River, Nevada: III. Effects on Blood and Organ Biochemistry and Histopathology of Snowy Egrets and Black-Crowned Night-Herons on Lahontan Reservoir, 2002–2006

A 10-year study (1997–2006) was conducted to evaluate reproduction and health of aquatic birds in the Carson River Basin of northwestern Nevada (on the U.S. Environmental Protection Agency Natural Priorities List) due to high mercury (Hg) concentrations from past mining activities. This part of the study evaluated physiological associations with blood Hg in young snowy egrets (Egretta thula) and black-crowned night-herons (Nycticorax nycticorax), and organ biochemistry and histopathological effects in snowy egrets on Lahontan Reservoir (LR) from the period 2002–2006. LR snowy egret geometric mean total Hg concentrations (µg/g ww) ranged from 1.5 to 4.8 for blood, 2.4 to 3.1 liver, 1.8 to 2.5 kidneys, 1.7 to 2.4 brain, and 20.5 to 36.4 feathers over these years. For night-herons, mean Hg for blood ranged from 1.6 to 7.4. Significant positive correlations were found between total Hg in blood and five plasma enzyme activities of snowy egrets suggesting hepatic stress. Histopathological findings revealed vacuolar changes in hepatocytes in LR snowy egrets as well as correlation of increased liver inflammation with increasing blood and tissue Hg. Hepatic oxidative effects were manifested by decreased hepatic total thiol concentration and glutathione reductase activity and elevated hepatic thiobarbituric acid-reactive subatances (TBARS), a measure of lipid peroxidation. However, other hepatic changes indicated compensatory mechanisms in response to oxidative stress, including decreased oxidized glutathione (GSSG) concentration and decreased ratio of GSSG to reduced glutathione. In young black-crowned night-herons, fewer correlations were apparent. In both species, positive correlations between blood total Hg and plasma uric acid and inorganic phosphorus were suggestive of renal stress, which was supported by histopathological findings. Both oxidative effects and adaptive responses to oxidative stress were apparent in kidneys and brain. Vacuolar change and inflammation in peripheral nerves were found to correlate with blood and tissue Hg. Hg-associated effects related to the immune system included alterations in specific white blood cells and lymphoid depletion in the bursa that were correlated with blood and tissue Hg. When the number of plasma variables that differed between young snowy egrets from the LR site and the reference site were compared between wet and drought years, over twice as many variables were affected during drought years. This resulted in many more variables correlating with blood total Hg during dry than during wet years, suggesting the combination of drought and Hg was more stressful than Hg alone. Drought may have exacerbated Hg-related effects as reported previously for overall productivity. This relationship was not evident in black-crowned night-herons, although data were more limited.

Intestinal helminths of river otters ( Lutra canadensis ) from the Pacific Northwest

The intestinal helminth fauna of river otters, Lutra canadensis, from the Pacific Northwest was characterized by low species richness and intensity of infection. River otters from the lower Columbia River (n = 23) were infected with 9 species of helminths (83% prevalence); those from a relatively undisturbed reference area near the headwaters of the Trask and Wilson rivers on the Oregon coast (n = 6) were infected by 5 species of helminths (100% prevalence). Single species of Eucestoda (Schistocephalus solidus), Digenea (Euparyphium inerme), Acanthocephala (Corynosoma strumosum), and 8 species of Nematoda (Strongyloides lutrae; larvae of Eustrongylides sp., Anisakis sp., and Contracaecum sp.; 3 of Cystidicolidae, and Hedruris sp.) were collected. Most species are typical of piscine definitive hosts and were present as incidental parasites of river otters. Notably, specimens of Euparyphium inerme are reported for the first time in river otters from North America; occurrence of other helminths constitutes new host or geographic records for parasites in river otters in Oregon and Washington. Parasites with marine life cycles were acquired by river otters in freshwater habitats at a great distance from the ocean. The helminth fauna of river otters in the Pacific Northwest was influenced primarily by ecological factors and was indicative of eclectic food habits and the relatively extensive home ranges occupied by these mustelids.

Effects of pelletized anticoagulant rodenticides on California quail.

A moribund, emaciated California quail (Callipepla californica) that was found in an orchard in the state of Washington had an impacted crop and gizzard. Pellets containing the anticoagulant chlorophacinone (Rozol®, RO) were in the crop; the gizzard contents consisted of a pink mass of paraffin that was selectively accumulated from the paraffinized pellets. The plasma prothrombin time of 28 sec was near that determined for control quail. The signs of RO intoxication seen in the moribund wild quail were duplicated in captive quail given ad libitum diets of either RO or another paraffinized chlorophacinone pellet (Mr. Rat Guard II®, MRG). This left little doubt that paraffin impaction of the gizzard was the primary problem. All captive quail fed RO or MRG pellets showed no increases in prothrombin times compared to control values, died in an emaciated condition, and had gizzards impacted with paraffin.

Health status of Largescale Sucker (Catostomus macrocheilus) collected along an organic contaminant gradient in the lower Columbia River, Oregon and Washington, USA

The health of Largescale Sucker (Catostomus macrocheilus) in the lower Columbia River (USA) was evaluated using morphometric and histopathological approaches, and its association with organic contaminants accumulated in liver was evaluated in males. Fish were sampled from three sites along a contaminant gradient. In 2009, body length and mass, condition factor, gonadosomatic index, and hematocrit were measured in males and females; liver and gonad tissue were collected from males for histological analyses; and organ composites were analyzed for contaminant content in males. In 2010, additional data were collected for males and females, including external fish condition assessment, histopathologies of spleen, kidney and gill and, for males, liver contaminant content. Multivariate analysis of variance indicated that biological traits in males, but not females, differed among sites in 2009 and 2010. Discriminant function analysis indicated that site-related differences among male populations were relatively small in 2009, but in 2010, when more variables were analyzed, males differed among sites in regards to kidney, spleen, and liver histopathologies and gill parasites. Kidney tubular hyperplasia, liver and spleen macrophage aggregations, and gill parasites were generally more severe in the downstream sites compared to the reference location. The contaminant content of male livers was also generally higher downstream, and the legacy pesticide hexachlorobenzene and flame retardants BDE-47 and BDE-154 were the primary drivers for site discrimination. However, bivariate correlations between biological variables and liver contaminants retained in the discriminant models failed to reveal associations between the two variable sets. In conclusion, whereas certain non-reproductive biological traits and liver contaminant contents of male Largescale Sucker differed according to an upstream-downstream gradient in the lower Columbia River, results from this study did not reveal the specific environmental factors responsible for the differences in health status among fish populations.

Bilateral Uric Acid Nephrolithiasis and Ureteral Hypertrophy in a Free-ranging River Otter (Lontra canadensis)

We report the first case of uric acid nephrolithiasis in a free-ranging river otter (Lontra canadensis). A 7 yr old male river otter collected from the Skagit River of western Washington (USA) had bilateral nephrolithiasis and severely enlarged ureters (one of 305 examined [0.33%]). The uroliths were 97% uric acid and 3% protein. Microscopic changes in the kidney were confined to expansion of renal calyces, minor loss of medullary tissue, and multifocal atrophy of the cortical tubules. No inflammation was observed in either kidney or the ureters. The ureters were enlarged due to marked hypertrophy of smooth muscle plus dilation of the lumen. Fusion of the major calyces into a single ureteral lumen was several cm distal to that of two adult male otters used as histopathologic control specimens. This case report is part of a large contaminant study of river otters collected from Oregon and Washington. It is important to understand diseases and lesions of the otter as part of our overall evaluation of this population.