Joshua T. Ackerman

Mercury demethylation in waterbird livers: Dose–response thresholds and differences among species

We assessed methylmercury (MeHg) demethylation in the livers of adults and chicks of four waterbird species that commonly breed in San Francisco Bay: American avocets, black-necked stilts, Caspian terns, and Forsters terns. In adults (all species combined), we found strong evidence for a threshold model where MeHg demethylation occurred above a hepatic total mercury concentration threshold of 8.51 +/- 0.93 microg/g dry weight, and there was a strong decline in %MeHg values as total mercury (THg) concentrations increased above 8.51 microg/g dry weight. Conversely, there was no evidence for a demethylation threshold in chicks, and we found that %MeHg values declined linearly with increasing THg concentrations. For adults, we also found taxonomic differences in the demethylation responses, with avocets and stilts showing a higher demethylation rate than that of terns when concentrations exceeded the threshold, whereas terns had a lower demethylation threshold (7.48 +/- 1.48 microg/g dry wt) than that of avocets and stilts (9.91 +/- 1.29 microg/g dry wt). Finally, we assessed the role of selenium (Se) in the demethylation process. Selenium concentrations were positively correlated with inorganic Hg in livers of birds above the demethylation threshold but not below. This suggests that Se may act as a binding site for demethylated Hg and may reduce the potential for secondary toxicity. Our findings indicate that waterbirds demethylate mercury in their livers if exposure exceeds a threshold value and suggest that taxonomic differences in demethylation ability may be an important factor in evaluating species-specific risk to MeHg exposure. Further, we provide strong evidence for a threshold of approximately 8.5 microg/g dry weight of THg in the liver where demethylation is initiated.

Effects of investigator disturbance on hatching success and nest-site fidelity in a long-lived seabird, Leach's storm-petrel

Abstract Long-lived animals are expected to reduce reproductive effort when breeding conditions are unfavorable, therefore seabirds may be especially sensitive to investigator disturbance. In a non-threatened procellariiform, Leachs storm-petrel Oceanodroma leucorhoa, we examined whether the frequency and the time of day of investigator disturbance influenced hatching success, and if disturbance affected hatching success and nest-site fidelity in the subsequent breeding season. Birds used in this study had received little or no investigator disturbance during the prior decade. Hatching success was significantly influenced by the frequency, but not the time of day, of disturbance. Weekly and daily handling of parents reduced hatching success by 50 and 56% compared to the control group. Most failures (91%) were caused by egg desertion, and all the deserted eggs belonged to pairs in the weekly and daily groups. During the subsequent breeding season, the hatching success of disturbed pairs that continued to breed together returned to normal levels. However, 37% more disturbed pairs than control pairs deserted the nesting burrows they had used in the previous year. Since most changes in nest site also result in mate change, investigator disturbance may have had long-term negative effects on reproductive success as well. Our results demonstrate that both weekly and daily investigator disturbance during incubation greatly reduced the hatching success and subsequent nest-site fidelity of naive Leachs storm-petrels.

Mercury bioaccumulation and risk to three waterbird foraging guilds is influenced by foraging ecology and breeding stage

We evaluated mercury (Hg) in five waterbird species representing three foraging guilds in San Francisco Bay, CA. Fish-eating birds (Forsters and Caspian terns) had the highest Hg concentrations in their tissues, but concentrations in an invertebrate-foraging shorebird (black-necked stilt) were also elevated. Foraging habitat was important for Hg exposure as illustrated by within-guild differences, where species more associated with marshes and salt ponds had higher concentrations than those more associated with open-bay and tidal mudflats. Importantly, Hg concentrations increased with time spent in the estuary. Surf scoter concentrations tripled over six months, whereas Forsters terns showed an up to 5-fold increase between estuary arrival and breeding. Breeding waterbirds were at elevated risk of Hg-induced reproductive impairment, particularly Forsters terns, in which 48% of breeding birds were at high risk due to their Hg levels. Our results highlight the importance of habitat and exposure timing, in addition to trophic position, on waterbird Hg bioaccumulation and risk.

Mercury correlations among six tissues for four waterbird species breeding in San Francisco Bay, California, USA†

Despite a large body of research concerning mercury (Hg) in birds, no single tissue has been used consistently to assess Hg exposure, and this has hampered comparisons across studies. We evaluated the relationships of Hg concentrations among tissues in four species of waterbirds (American avocets [Recurvirostra americana], black-necked stilts [Himantopus mexicanus], Caspian terns [Hydroprogne caspia; formerly Sterna caspia], and Forsters terns [Sterna forsteri]) and across three life stages (prebreeding adults, breeding adults, and chicks) in San Francisco Bay, California, USA. Across species and life stages, Hg concentrations (least square mean +/- standard error) were highest in head feathers (6.45 +/- 0.31 microg/g dry wt) and breast feathers (5.76 +/- 0.28 microg/g dry wt), followed by kidney (4.54 +/- 0.22 microg/g dry wt), liver (4.43 +/- 0.21 microg/g dry wt), blood (3.10 +/- 0.15 microg/g dry wt), and muscle (1.67 +/- 0.08 microg/g dry wt). Relative Hg distribution among tissues, however, differed by species and life stage. Mercury concentrations were highly correlated among internal tissues (r2 > or = 0.89). Conversely, the relationships between Hg in feathers and internal tissues were substantially weaker (r2 < or = 0.42). Regression slopes sometimes differed among species and life stages, indicating that care must be used when predicting Hg concentrations in one tissue based on those in another. However, we found good agreement between predictions made using a general tissue-prediction equation and more specific equations developed for each species and life stage. Finally, our results suggest that blood is an excellent, nonlethal predictor of Hg concentrations in internal tissues but that feathers are relatively poor indicators of Hg concentrations in internal tissues.

Mercury cycling in agricultural and managed wetlands: A synthesis of methylmercury production, hydrologic export, and bioaccumulation from an integrated field study

With seasonal wetting and drying, and high biological productivity, agricultural wetlands (rice paddies) may enhance the conversion of inorganic mercury (Hg(II)) to methylmercury (MeHg), the more toxic, organic form that biomagnifies through food webs. Yet, the net balance of MeHg sources and sinks in seasonal wetland environments is poorly understood because it requires an annual, integrated assessment across biota, sediment, and water components. We examined a suite of wetlands managed for rice crops or wildlife during 2007-2008 in Californias Central Valley, in an area affected by Hg contamination from historic mining practices. Hydrologic management of agricultural wetlands for rice, wild rice, or fallowed - drying for field preparation and harvest, and flooding for crop growth and post-harvest rice straw decay - led to pronounced seasonality in sediment and aqueous MeHg concentrations that were up to 95-fold higher than those measured concurrently in adjacent, non-agricultural permanently-flooded and seasonally-flooded wetlands. Flooding promoted microbial MeHg production in surface sediment of all wetlands, but extended water residence time appeared to preferentially enhance MeHg degradation and storage. When incoming MeHg loads were elevated, individual fields often served as a MeHg sink, rather than a source. Slow, horizontal flow of shallow water in the agricultural wetlands led to increased importance of vertical hydrologic fluxes, including evapoconcentration of surface water MeHg and transpiration-driven advection into the root zone, promoting temporary soil storage of MeHg. Although this hydrology limited MeHg export from wetlands, it also increased MeHg exposure to resident fish via greater in situ aqueous MeHg concentrations. Our results suggest that the combined traits of agricultural wetlands - slow-moving shallow water, manipulated flooding and drying, abundant labile plant matter, and management for wildlife - may enhance microbial methylation of Hg(II) and MeHg exposure to local biota, as well as export to downstream habitats during uncontrolled winter-flow events.

Mercury concentrations in blood and feathers of prebreeding forster's terns in relation to space use of san francisco bay, california, usa, habitats†

We examined mercury concentrations and space use of prebreeding Forsters terns (Sterna forsteri) in San Francisco Bay, California, USA, to assess factors influencing mercury levels in piscivorous birds. In 2005 and 2006, we collected blood and feathers from 122 Forsters terns and radio-marked and tracked 72 terns to determine locations of dietary mercury uptake. Capture site and capture date were the most important factors explaining variation in blood mercury concentrations (geometric mean +/- standard error: 1.09+/-0.89 microg/g wet wt), followed by sex and year. Accordingly, radiotelemetry data revealed that Forsters terns generally remained near their site of capture and foraged in nearby salt ponds, managed and tidal marshes, and tidal flats. In contrast, capture site and capture date were not important factors explaining variation in feather mercury concentrations, probably because feathers were grown on their wintering grounds several months prior to our sampling. Instead, sex and year were the most important factors explaining mercury concentrations in breast feathers (9.57+/-8.23 microg/g fresh wt), and sex was the most important factor for head feathers (6.94+/-7.04 microg/g fresh wt). Overall, 13 and 22% of prebreeding Forsters terns were estimated to be at high risk for deleterious effects due to mercury concentrations in blood (>3.0 microg/g wet wt) and feathers (>20.0 microg/g fresh wt), respectively. Breeding terns are likely to be even more at risk because blood mercury concentrations more than tripled during the 45-d prebreeding time period. These data illustrate the importance of space use and tissue type in interpreting mercury concentrations in birds.

Spatial use by wintering greater white-fronted geese relative to a decade of habitat change in California's central valley

Abstract We investigated the effect of recent habitat changes in Californias Central Valley on wintering Pacific greater white-fronted geese (Anser albifrons frontalis) by comparing roost-to-feed distances, distributions, population range sizes, and habitat use during 1987–1990 and 1998–2000. These habitat changes included wetland restoration and agricultural land enhancement due to the 1990 implementation of the Central Valley Joint Venture, increased land area used for rice (Oryza sativa) production, and the practice of flooding, rather than burning, rice straw residues for decomposition because of burning restrictions enacted in 1991. Using radiotelemetry, we tracked 192 female geese and recorded 4,516 locations. Geese traveled shorter distances between roosting and feeding sites during 1998–2000 (24.2 ± 2.2 km) than during 1987–1990 (32.5 ± 3.4 km); distance traveled tended to decline throughout winter during both decades and varied among watershed basins. Population range size was smaller during 1998–2000 (3,367 km2) than during 1987–1990 (5,145 km2), despite a 2.2-fold increase in the size of the Pacific Flyway population of white-fronted geese during the same time period. The population range size also tended to increase throughout winter during both decades. Feeding and roosting distributions of geese also differed between decades; geese shifted into basins that had the greatest increases in the amount of area in rice production (i.e., American Basin) and out of other basins (i.e., Delta Basin). The use of rice habitat for roosting (1987–1990: 40%, 1998–2000: 54%) and feeding (1987–1990: 57%, 1998–2000: 72%) increased between decades, whereas use of wetlands declined for roosting (1987–1990: 36%, 1998–2000: 31%) and feeding (1987–1990: 22%, 1998–2000: 12%). Within postharvested rice habitats, geese roosted and fed primarily in burned rice fields during 1987–1990 (roost: 43%, feed: 34%), whereas they used flooded rice fields during 1998–2000 (roost: 78%, feed: 64%). Our results suggest that white-fronted geese have altered their spatial use of Californias Central Valley during the past decade in response to changing agricultural practices and the implementation of the Central Valley Joint Venture.

Bird Mercury Concentrations Change Rapidly as Chicks Age: Toxicological Risk is Highest at Hatching and Fledging

Toxicological risk of methylmercury exposure to juvenile birds is complex due to the highly transient nature of mercury concentrations as chicks age. We examined total mercury and methylmercury concentrations in blood, liver, kidney, muscle, and feathers of 111 Forsters tern (Sterna forsteri), 69 black-necked stilt (Himantopus mexicanus), and 43 American avocet (Recurvirostra americana) chicks as they aged from hatching through postfledging at wetlands that had either low or high mercury contamination in San Francisco Bay, California. For each waterbird species, internal tissue, and wetland, total mercury and methylmercury concentrations changed rapidly as chicks aged and exhibited a quadratic, U-shaped pattern from hatching through postfledging. Mercury concentrations were highest immediately after hatching, due to maternally deposited mercury in eggs, then rapidly declined as chicks aged and diluted their mercury body burden through growth in size and mercury depuration into growing feathers. Mercury concentrations then increased during fledging when mass gain and feather growth slowed, while chicks continued to acquire dietary mercury. In contrast to mercury in internal tissues, mercury concentrations in chick feathers were highly variable and declined linearly with age. For 58 recaptured Forsters tern chicks, the proportional change in blood mercury concentration was negatively related to the proportional change in body mass, but not to the amount of feathers or wing length. Thus, mercury concentrations declined more in chicks that gained more mass between sampling events. The U-shaped pattern of mercury concentrations from hatching to fledging indicates that juvenile birds may be at highest risk to methylmercury toxicity shortly after hatching when maternally deposited mercury concentrations are still high and again after fledging when opportunities for mass dilution and mercury excretion into feathers are limited.

Migration strategy affects avian influenza dynamics in mallards (Anas platyrhynchos)

Studies of pathogen transmission typically overlook that wildlife hosts can include both migrant and resident populations when attempting to model circulation. Through the application of stable isotopes in flight feathers, we estimated the migration strategy of mallards (Anas platyrhynchos) occurring on California wintering grounds. Our study demonstrates that mallards‐ a principal host of avian influenza virus (AIV) in nature, contribute differently to virus gene flow depending on migration strategy. No difference in AIV prevalence was detected between resident (9.6%), intermediate‐distance (9.6%) and long‐distance migrants (7.4%). Viral diversity among the three groups was also comparable, possibly owing to viral pool mixing when birds converge at wetlands during winter. However, migrants and residents contributed differently to the virus gene pool at wintering wetlands. Migrants introduced virus from northern breeding grounds (Alaska and the NW Pacific Rim) into the wintering population, facilitating gene flow at continental scales, but circulation of imported virus appeared to be limited. In contrast, resident mallards acted as AIV reservoirs facilitating year‐round circulation of limited subtypes (i.e. H5N2) at lower latitudes. This study supports a model of virus exchange in temperate regions driven by the convergence of wild birds with separate geographic origins and exposure histories.

Effects of radiotransmitters on the reproductive performance of Cassin’s auklets

Abstract We examined whether radiotransmitters adversely affected the reproductive performance of Cassin’s auklets (Ptychoramphus aleuticus) breeding on the California Channel Islands during 1999-2001. We attached external radiotransmitters to 1 partner in 108 Cassin’s auklet pairs after nest initiation and used 131 unmarked, but handled, pairs as controls. Compared to alpha chicks raised by radiomarked pairs, alpha chicks raised by unmarked pairs had faster mass growth rates (1.95 ± 0.30 g d-1 vs. 3.37 ± 0.53 g d-1, respectively), faster wing growth rates (2.46 ± 0.10 mm d-1 vs. 2.85 ± 0.05 mm d-1), greater peak fledging masses (118.9 ± 3.5 g vs. 148.3 ± 2.4 g), and higher fledging success (61% vs. 90%). Fledging success was reduced more when we radiomarked the male (50% fledged) rather than the female partner (77% fledged). After fledging an alpha chick, unmarked pairs were more likely to initiate a second clutch (radiomarked: 7%; unmarked: 39%) but did not hatch a second egg (radiomarked: 4%; unmarked: 25%) or fledge a second (beta) chick (radiomarked: 4%; unmarked: 18%) significantly more often than radiomarked pairs. We resighted 12 radiomarked individuals nesting during a subsequent breeding season; each bird had shed its transmitter and healed the site of attachment. We suggest caution in using telemetry to evaluate the reproductive performance of alcids, but marking only females may minimize adverse effects.