Methylmercury Effects on Birds: A Review, Meta-Analysis, and Development of Toxicity Reference Values for Injury Assessment Based on Tissue Residues and Diet.

Birds are used as bioindicators of environmental mercury (Hg) contamination, and toxicity reference values are needed for injury assessments. We conducted a comprehensive review, summarized data from 168 studies, performed a series of Bayesian hierarchical meta-analyses, and developed new toxicity reference values for the effects of methylmercury (MeHg) on birds using a benchmark dose analysis framework. Lethal and sublethal effects of MeHg on birds were categorized into nine biologically relevant endpoint categories and three age classes. Effective Hg concentrations where there was a 10% reduction (EC10) in the production of juvenile offspring (0.55 µg/g wet wt adult blood-equivalent Hg concentrations, 80% credible interval: [0.33, 0.85]), histology endpoints (0.49 [0.15, 0.96] and 0.61 [0.09, 2.48]), and biochemical markers (0.77 [<0.25, 2.12] and 0.57 [0.35, 0.92]) were substantially lower than those for survival (2.97 [2.10, 4.73] and 5.24 [3.30, 9.55]) and behavior (6.23 [1.84, >13.42] and 3.11 [2.10, 4.64]) of juveniles and adults, respectively. Within the egg age class, survival was the most sensitive endpoint (EC10 = 2.02 µg/g wet wt adult blood-equivalent Hg concentrations [1.39, 2.94] or 1.17 µg/g fresh wet wt egg-equivalent Hg concentrations [0.80, 1.70]). Body morphology was not particularly sensitive to Hg. We developed toxicity reference values using a combined survival and reproduction endpoints category for juveniles, because juveniles were more sensitive to Hg toxicity than eggs or adults. Adult blood-equivalent Hg concentrations (µg/g wet wt) and egg-equivalent Hg concentrations (µg/g fresh wet wt) caused low injury to birds (EC1) at 0.09 [0.04, 0.17] and 0.04 [0.01, 0.08], moderate injury (EC5) at 0.6 [0.37, 0.84] and 0.3 [0.17, 0.44], high injury (EC10) at 1.3 [0.94, 1.89] and 0.7 [0.49, 1.02], and severe injury (EC20) at 3.2 [2.24, 4.78] and 1.8 [1.28, 2.79], respectively. Maternal dietary Hg (µg/g dry wt) caused low injury to juveniles at 0.16 [0.05, 0.38], moderate injury at 0.6 [0.29, 1.03], high injury at 1.1 [0.63, 1.87], and severe injury at 2.4 [1.42, 4.13]. We found few substantial differences in Hg toxicity among avian taxonomic orders, including for controlled laboratory studies that injected Hg into eggs. Our results can be used to quantify injury to birds caused by Hg pollution. Environ Toxicol Chem 2024;43:1195-1241. Published 2024. This article is a U.S. Government work and is in the public domain in the USA. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

Foraging behavior and age affect maternal transfer of mercury to northern elephant seal pups.

Deep ocean foraging northern elephant seals (Mirounga angustirostris) consume fish and squid in remote depths of the North Pacific Ocean. Contaminants bioaccumulated from prey are subsequently transferred by adult females to pups during gestation and lactation, linking pups to mercury contamination in mesopelagic food webs (200-1000 m depths). Maternal transfer of mercury to developing seal pups was related to maternal mercury contamination and was strongly correlated with maternal foraging behavior (biotelemetry and isotopes). Mercury concentrations in lanugo (hair grown in utero) were among the highest observed worldwide for young pinnipeds (geometric mean 23.01 µg/g dw, range 8.03-63.09 µg/g dw; n = 373); thus, some pups may be at an elevated risk of sub-lethal adverse health effects. Fetal mercury exposure was affected by maternal foraging geographic location and depth; mercury concentrations were highest in pups of the deepest diving, pelagic females. Moreover, pup lanugo mercury concentrations were strongly repeatable among successive pups of individual females, demonstrating relative consistency in pup mercury exposure based on maternal foraging strategies. Northern elephant seals are biosentinels of a remote deep-sea ecosystem. Our results suggest that mercury within North Pacific mesopelagic food webs may also pose an elevated risk to other mesopelagic-foraging predators and their offspring.

Nest attendance, incubation constancy, and onset of incubation in dabbling ducks.

In birds, parents must provide their eggs with a safe thermal environment suitable for embryonic development. Species with uniparental incubation must balance time spent incubating eggs with time spent away from the nest to satisfy self-maintenance needs. Patterns of nest attendance, therefore, influence embryonic development and the time it takes for eggs to hatch. We studied nest attendance (time on the nest), incubation constancy (time nests were at incubation temperatures), and variation in nest temperature of 1,414 dabbling duck nests of three species in northern California. Daily nest attendance increased from only 1-3% on the day the first egg was laid to 51-57% on the day of clutch completion, and 80-83% after clutch completion through hatch. Variation in nest temperature also decreased gradually during egg-laying, and then dropped sharply (33-38%) between the day of and the day after clutch completion because increased nest attendance, particularly at night, resulted in more consistent nest temperatures. During the egg-laying stage, nocturnal nest attendance was low (13-25%), whereas after clutch completion, nest attendance was greater at night (≥87%) than during the day (70-77%) because most incubation recesses occurred during the day. Moreover, during egg-laying, nest attendance and incubation constancy increased more slowly among nests with larger final clutch sizes, suggesting that the number of eggs remaining to be laid is a major driver of incubation effort during egg-laying. Although overall nest attendance after clutch completion was similar among species, the average length of individual incubation bouts was greatest among gadwall (Mareca strepera; 779 minutes), followed by mallard (Anas platyrhynchos; 636 minutes) and then cinnamon teal (Spatula cyanoptera; 347 minutes). These results demonstrate that dabbling ducks moderate their incubation behavior according to nest stage, nest age, time of day, and clutch size and this moderation likely has important implications for egg development and overall nest success.

Mercury Bioaccumulation and Cortisol Interact to Influence Endocrine and Immune Biomarkers in a Free-Ranging Marine Mammal.

Mercury bioaccumulation from deep-ocean prey and the extreme life history strategies of adult female northern elephant seals (Mirounga angustirostris) provide a unique system to assess the interactive effects of mercury and stress on animal health by quantifying blood biomarkers in relation to mercury (skeletal muscle and blood mercury) and cortisol concentrations. The thyroid hormone thyroxine (tT4) and the antibody immunoglobulin E (IgE) were associated with mercury and cortisol concentrations interactively, where the magnitude and direction of the association of each biomarker with mercury or cortisol changed depending on the concentration of the other factor. For example, when cortisol concentrations were lowest, tT4 was positively related to muscle mercury, whereas tT4 had a negative relationship with muscle mercury in seals that had the highest cortisol concentrations. Additionally, we observed that two thyroid hormones, triiodothyronine (tT3) and reverse triiodothyronine (rT3), were negatively (tT3) and positively (rT3) associated with mercury concentrations and cortisol in an additive manner. As an example, tT3 concentrations in late breeding seals at the median cortisol concentration decreased by 14% across the range of observed muscle mercury concentrations. We also observed that immunoglobulin M (IgM), the pro-inflammatory cytokine IL-6 (IL-6), and a reproductive hormone, estradiol, were negatively related to muscle mercury concentrations but were not related to cortisol. Specifically, estradiol concentrations in late molting seals decreased by 50% across the range of muscle mercury concentrations. These results indicate important physiological effects of mercury on free-ranging apex marine predators and interactions between mercury bioaccumulation and extrinsic stressors. Deleterious effects on animals' abilities to maintain homeostasis (thyroid hormones), fight off pathogens and disease (innate and adaptive immune system), and successfully reproduce (endocrine system) can have significant individual- and population-level consequences.

Predator movements in relation to habitat features reveal vulnerability of duck nests to predation.

Nest predation is the main cause of nest failure for ducks. Understanding how habitat features influence predator movements may facilitate management of upland and wetland breeding habitats that reduces predator encounter rates with duck nests and increases nest survival rates. For 1618 duck nests, nest survival increased with distance to phragmites (Phragmites australis), shrubs, telephone poles, human structures, and canals, but not for four other habitat features. Using GPS collars, we tracked 25 raccoons (Procyon lotor) and 16 striped skunks (Mephitis mephitis) over 4 years during waterfowl breeding and found marked differences in how these predators were located relative to specific habitat features; moreover, the probability of duck nests being encountered by predators differed by species. Specifically, proximity to canals, wetlands, trees, levees/roads, human structures, shrubs, and telephone poles increased the likelihood of a nest being encountered by collared raccoons. For collared skunks, nests were more likely to be encountered if they were closer to canals, trees, and shrubs, and farther from wetlands and human structures. Most predator encounters with duck nests were attributable to a few individuals; 29.2% of raccoons and 38.5% of skunks were responsible for 95.6% of total nest encounters. During the central span of duck nesting (April 17-June 14: 58 nights), these seven raccoons and five skunks encountered >1 nest on 50.8 ± 29.2% (mean ± SD) and 41.5 ± 28.3% of nights, respectively, and of those nights individual raccoons and skunks averaged 2.60 ± 1.28 and 2.50 ± 1.09 nest encounters/night, respectively. For collared predators that encountered >1 nest, a higher proportion of nests encountered by skunks had evidence of predation (51.9 ± 26.6%) compared to nests encountered by raccoons (22.3 ± 17.1%). Because duck eggs were most likely consumed as raccoons and skunks opportunistically discovered nests, managing the habitat features those predators most strongly associated with could potentially reduce rates of egg predation.

Avian influenza antibody prevalence increases with mercury contamination in wild waterfowl.

Environmental contamination is widespread and can negatively impact wildlife health. Some contaminants, including heavy metals, have immunosuppressive effects, but prior studies have rarely measured contamination and disease simultaneously, which limits our understanding of how contaminants and pathogens interact to influence wildlife health. Here, we measured mercury concentrations, influenza infection, influenza antibodies and body condition in 749 individuals from 11 species of wild ducks overwintering in California. We found that the odds of prior influenza infection increased more than fivefold across the observed range of blood mercury concentrations, while accounting for species, age, sex and date. Influenza infection prevalence was also higher in species with higher average mercury concentrations. We detected no relationship between influenza infection and body fat content. This positive relationship between influenza prevalence and mercury concentrations in migratory waterfowl suggests that immunotoxic effects of mercury contamination could promote the spread of avian influenza along migratory flyways, especially if influenza has minimal effects on bird health and mobility. More generally, these results show that the effects of environmental contamination could extend beyond the geographical area of contamination itself by altering the prevalence of infectious diseases in highly mobile hosts.

Nocturnal incubation recess and flushing behavior by duck hens.

Incubating birds must balance the needs of their developing embryos with their own physiological needs, and many birds accomplish this by taking periodic breaks from incubation. Mallard (Anas platyrhynchos) and gadwall (Mareca strepera) hens typically take incubation recesses in the early morning and late afternoon, but recesses can also take place at night. We examined nocturnal incubation recess behavior for mallard and gadwall hens nesting in Suisun Marsh, California, USA, using iButton temperature dataloggers and continuous video monitoring at nests. Fourteen percent of all detected incubation recesses (N = 13,708) were nocturnal and took place on 20% of nest-days (N = 8,668). Video monitoring showed that hens covered their eggs with down feathers when they initiated a nocturnal recess themselves as they would a diurnal recess, but they left the eggs uncovered in 94% of the nocturnal recesses in which predators appeared at nests. Thus, determining whether or not eggs were left uncovered during a recess can provide strong indication whether the recess was initiated by the hen (eggs covered) or a predator (eggs uncovered). Because nest temperature decreased more rapidly when eggs were left uncovered versus covered, we were able to characterize eggs during nocturnal incubation recesses as covered or uncovered using nest temperature data. Overall, we predicted that 75% of nocturnal recesses were hen-initiated recesses (eggs covered) whereas 25% of nocturnal recesses were predator-initiated recesses (eggs uncovered). Of the predator-initiated nocturnal recesses, 56% were accompanied by evidence of depredation at the nest during the subsequent nest monitoring visit. Hen-initiated nocturnal recesses began later in the night (closer to morning) and were shorter than predator-initiated nocturnal recesses. Our results indicate that nocturnal incubation recesses occur regularly (14% of all recesses) and, similar to diurnal recesses, most nocturnal recesses (75%) are initiated by the hen rather than an approaching predator.

Forced into an ecological corner: Round-the-clock deep foraging on small prey by elephant seals.

Small mesopelagic fishes dominate the world's total fish biomass, yet their ecological importance as prey for large marine animals is poorly understood. To reveal the little-known ecosystem dynamics, we identified prey, measured feeding events, and quantified the daily energy balance of 48 deep-diving elephant seals throughout their oceanic migrations by leveraging innovative technologies: animal-borne smart accelerometers and video cameras. Seals only attained positive energy balance after feeding 1000 to 2000 times per day on small fishes, which required continuous deep diving (80 to 100% of each day). Interspecies allometry suggests that female elephant seals have exceptional diving abilities relative to their body size, enabling them to exploit a unique foraging niche on small but abundant mesopelagic fish. This unique foraging niche requires extreme round-the-clock deep diving, limiting the behavioral plasticity of elephant seals to a changing mesopelagic ecosystem.

Interrupted incubation: How dabbling ducks respond when flushed from the nest.

Nesting birds must provide a thermal environment sufficient for egg development while also meeting self-maintenance needs. Many birds, particularly those with uniparental incubation, achieve this balance through periodic incubation recesses, during which foraging and other self-maintenance activities can occur. However, incubating birds may experience disturbances such as predator or human activity which interrupt natural incubation patterns by compelling them to leave the nest. We characterized incubating mallard Anas platyrhynchos and gadwall Mareca strepera hens' responses when flushed by predators and investigators in Suisun Marsh, California, USA. Diurnal incubation recesses initiated by investigators approaching nests were 63% longer than natural diurnal incubation recesses initiated by the hen (geometric mean: 226.77 min versus 142.04 min). Nocturnal incubation recesses, many of which were likely the result of predators flushing hens, were of similar duration regardless of whether the nest was partially depredated during the event (115.33 [101.01;131.68] minutes) or not (119.62 [111.96;127.82] minutes), yet were 16% shorter than natural diurnal incubation recesses. Hens moved further from the nest during natural diurnal recesses or investigator-initiated recesses than during nocturnal recesses, and the proportion of hen locations recorded in wetland versus upland habitat during recesses varied with recess type (model-predicted means: natural diurnal recess 0.77; investigator-initiated recess 0.82; nocturnal recess 0.31). Hens were more likely to take a natural recess following an investigator-initiated recess earlier that same day than following a natural recess earlier that same day, and natural recesses that followed an investigator-initiated recess were longer than natural recesses that followed an earlier natural recess, suggesting that hens may not fulfill all of their physiological needs during investigator-initiated recesses. We found no evidence that the duration of investigator-initiated recesses was influenced by repeated visits to the nest, whether by predators or by investigators, and trapping and handling the hen did not affect investigator-initiated recess duration unless the hen was also fitted with a backpack-harness style GPS-GSM transmitter at the time of capture. Hens that were captured and fitted with GPS-GSM transmitters took recesses that were 26% longer than recesses during which a hen was captured but a GPS-GSM transmitter was not attached. Incubation interruptions had measurable but limited and specific effects on hen behavior.

Avian eggshell thickness in relation to egg morphometrics, embryonic development, and mercury contamination.

Eggshell thickness is important for physiological, ecological, and ecotoxicological studies on birds; however, empirical eggshell thickness measurements for many species and regions are limited. We measured eggshell thickness at the equator and the egg poles for 12 avian species and related eggshell thickness to egg morphometrics, embryonic development, egg status, and mercury contamination. Within an egg, eggshells were approximately 5.1% thicker at the equator than the sharp pole of the egg, although this difference varied among species (0.6%-9.8%). Within Forster's tern (Sterna forsteri), where eggshell thickness was measured at 5 equally spaced positions along the longitude of the egg, eggshell thickness changed more rapidly near the sharp pole of the egg compared to near the blunt pole of the egg. Within species, eggshell thickness was related to egg width and egg volume for six of the 12 species but was not related to egg length for any species. Among species, mean eggshell thickness was strongly related to species mean egg width, egg length, egg volume, and bird body mass, although species mean body mass was the strongest predictor of species mean eggshell thickness. Using three species (American avocet [Recurvirostra americana], black-necked stilt [Himantopus mexicanus], and Forster's tern), whose nests were carefully monitored, eggshell thickness (including the eggshell membrane) did not differ among viable, naturally abandoned, dead, or failed-to-hatch eggs; was not related to total mercury concentrations of the egg content; and did not decrease with embryonic age. Our study also provides a review of all existing eggshell thickness data for these 12 species.

Acceleration-triggered animal-borne videos show a dominance of fish in the diet of female northern elephant seals.

Knowledge of the diet of marine mammals is fundamental to understanding their role in marine ecosystems and response to environmental change. Recently, animal-borne video cameras have revealed the diet of marine mammals that make short foraging trips. However, novel approaches that allocate video time to target prey capture events is required to obtain diet information for species that make long foraging trips over great distances. We combined satellite telemetry and depth recorders with newly developed date-/time-, depth- and acceleration-triggered animal-borne video cameras to examine the diet of female northern elephant seals during their foraging migrations across the eastern North Pacific. We obtained 48.2 h of underwater video, from cameras mounted on the head (n=12) and jaw (n=3) of seals. Fish dominated the diet (78% of 697 prey items recorded) across all foraging locations (range: 37-55°N, 122-152°W), diving depths (range: 238-1167 m) and water temperatures (range: 3.2-7.4°C), while squid comprised only 7% of the diet. Identified prey included fish such as myctophids, Merluccius sp. and Icosteus aenigmaticus, and squid such as Histioteuthis sp., Octopoteuthis sp. and Taningia danae Our results corroborate fatty acid analysis, which also found that fish are more important in the diet, and are in contrast to stomach content analyses that found cephalopods to be the most important component of the diet. Our work shows that in situ video observation is a useful method for studying the at-sea diet of long-ranging marine predators.

Mercury exposure in mammalian mesopredators inhabiting a brackish marsh.

Bioaccumulation of environmental contaminants in mammalian predators can serve as an indicator of ecosystem health. We examined mercury concentrations of raccoons (Procyon lotor; n = 37 individuals) and striped skunks (Mephitis mephitis; n = 87 individuals) in Suisun Marsh, California, a large brackish marsh that is characterized by contiguous tracts of tidal marsh and seasonally impounded wetlands. Mean (standard error; range) total mercury concentrations in adult hair grown from 2015 to 2018 were 28.50 µg/g dw (3.05 µg/g dw; range: 4.46-81.01 µg/g dw) in raccoons and 4.85 µg/g dw (0.54 µg/g dw; range: 1.53-27.02 µg/g dw) in striped skunks. We reviewed mammalian hair mercury concentrations in the literature and raccoon mercury concentrations in Suisun Marsh were among the highest observed for wild mammals. Although striped skunk hair mercury concentrations were 83% lower than raccoons, they were higher than proposed background levels for mercury in mesopredator hair (1-5 µg/g). Hair mercury concentrations in skunks and raccoons were not related to animal size, but mercury concentrations were higher in skunks in poorer body condition. Large inter-annual differences in hair mercury concentrations suggest that methylmercury exposure to mammalian predators varied among years. Mercury concentrations of raccoon hair grown in 2017 were 2.7 times greater than hair grown in 2015, 1.7 times greater than hair grown in 2016, and 1.6 times greater than hair grown in 2018. Annual mean raccoon and skunk hair mercury concentrations increased with wetland habitat area. Furthermore, during 2017, raccoon hair mercury concentrations increased with the proportion of raccoon home ranges that was wetted habitat, as quantified using global positioning system (GPS) collars. The elevated mercury concentrations we observed in raccoons and skunks suggest that other wildlife at similar or higher trophic positions may also be exposed to elevated methylmercury bioaccumulation in brackish marshes.

Sitting ducklings: Timing of hatch, nest departure, and predation risk for dabbling duck broods.

For ground-nesting waterfowl, the timing of egg hatch and duckling departure from the nest may be influenced by the risk of predation at the nest and en route to wetlands and constrained by the time required for ducklings to imprint on the hen and be physically able to leave the nest. We determined the timing of hatch, nest departure, and predation on dabbling duck broods using small video cameras placed at the nests of mallard (Anas platyrhynchos; n = 26), gadwall (Mareca strepera; n = 24), and cinnamon teal (Anas cyanoptera; n = 5). Mallard eggs began to hatch throughout the day and night, whereas gadwall eggs generally started to hatch during daylight hours (mean 7.5 hr after dawn). Among all species, duckling departure from the nest occurred during daylight (98%), and 53% of hens typically left the nest with their broods 1-4 hr after dawn. For mallard and gadwall, we identified three strategies for the timing of nest departure: (a) 9% of broods left the nest the same day that eggs began to hatch (6-12 hr later), (b) 81% of broods left the nest the day after eggs began to hatch, and (c) 10% of broods waited 2 days to depart the nest after eggs began to hatch, leaving the nest just after the second dawn (27-42 hr later). Overall, eggs were depredated at 10% of nests with cameras in the 2 days prior to hatch and ducklings were depredated at 15% of nests with cameras before leaving the nest. Our results suggest that broods prefer to depart the nest early in the morning, which may best balance developmental constraints with predation risk both at the nest and en route to wetlands.

GPS tracking data reveals daily spatio-temporal movement patterns of waterfowl.

BACKGROUND: Spatio-temporal patterns of movement can characterize relationships between organisms and their surroundings, and address gaps in our understanding of species ecology, activity budgets, bioenergetics, and habitat resource management. Highly mobile waterfowl, which can exploit resources over large spatial extents, are excellent models to understand relationships between movements and resource usage, landscape interactions and specific habitat needs. METHODS: We tracked 3 species of dabbling ducks with GPS-GSM transmitters in 2015-17 to examine fine-scale movement patterns over 24 h periods (30 min interval), dividing movement pathways into temporally continuous segments and spatially contiguous patches. We quantified distances moved, area used and time allocated across the day, using linear and generalized linear mixed models. We investigated behavior through relationships between these variables. RESULTS: Movements and space-use were small, and varied by species, sex and season. Gadwall (Mareca strepera) generally moved least (FFDs: 0.5-0.7 km), but their larger foraging patches resulted from longer within-area movements. Pintails (Anas acuta) moved most, were more likely to conduct flights > 300 m, had FFDs of 0.8-1.1 km, used more segments and patches per day that they revisited more frequently, resulting in the longest daily total movements. Females and males differed only during the post-hunt season when females moved more. 23.6% of track segments were short duration (1-2 locations), approximately 1/3 more than would be expected if they occurred randomly, and were more dispersed in the landscape than longer segments. Distance moved in 30 min shortened as segment duration increased, likely reflecting phases of non-movement captured within segments. CONCLUSIONS: Pacific Flyway ducks spend the majority of time using smaller foraging and resting areas than expected or previously reported, implying that foraging areas may be highly localized, and nutrients obtainable from smaller areas. Additionally, movement reductions over time demonstrates behavioral adjustments that represent divergent energetic demands, the detection of which is a key advantage of higher frequency data. Ducks likely use less energy for movement than currently predicted and management, including distribution and configuration of essential habitat, may require reconsideration. Our study illustrates how fine-scale movement data from tracking help understand and inform various other fields of research.

Mercury Concentrations Vary Within and Among Individual Bird Feathers: A Critical Evaluation and Guidelines for Feather Use in Mercury Monitoring Programs.

Feathers are widely used to represent mercury contamination in birds. Yet, few recommendations exist that provide guidance for using bird feathers in mercury monitoring programs. We conducted a literature review and 5 experiments to show that mercury concentrations vary substantially within (vane >100% higher than calamus) and among (>1000%) individual feathers from the same bird. We developed a research tool and guidelines for using bird feathers for mercury studies based on 3 components: 1) variability of feather mercury concentrations within an individual bird (coefficient of variation), 2) desired accuracy of the measured mercury concentration, and 3) feather and bird mass. Our results suggest a general rule that if the goal is to limit analytical and processing costs by using whole feathers in only one sample boat, then to achieve an accuracy within 10% of a bird's overall average feather mercury concentration a bird with a coefficient of variation ≤10% must be <190 g (size of a large shorebird). To achieve an accuracy within 20%, a bird with a coefficient of variation ≤10% must be <920 g (a large duck). When more than one sample boat is needed to fit the required number of feathers to achieve the desired accuracy, the results suggest homogenizing feathers and analyzing an aliquot of ≥20 mg for mercury. The present study suggests increasing the number of feathers typically used per bird to assess mercury concentrations. Environ Toxicol Chem 2019;38:1164-1187. Published 2019 Wiley Periodicals Inc. on behalf of SETAC. This article is a US government work and, as such, is in the public domain in the United States of America.

The energetic consequences of behavioral variation in a marine carnivore.

Intraspecific variability in foraging behavior has been documented across a range of taxonomic groups, yet the energetic consequences of this variation are not well understood for many species. Understanding the effect of behavioral variation on energy expenditure and acquisition is particularly crucial for mammalian carnivores because they have high energy requirements that place considerable pressure on prey populations. To determine the influence of behavior on energy expenditure and balance, we combined simultaneous measurements of at-sea field metabolic rate (FMR) and foraging behavior in a marine carnivore that exhibits intraspecific behavioral variation, the California sea lion (Zalophus californianus). Sea lions exhibited variability in at-sea FMR, with some individuals expending energy at a maximum of twice the rate of others. This variation was in part attributable to differences in diving behavior that may have been reflective of diet; however, this was only true for sea lions using a foraging strategy consisting of epipelagic (<200 m within the water column) and benthic dives. In contrast, sea lions that used a deep-diving foraging strategy all had similar values of at-sea FMR that were unrelated to diving behavior. Energy intake did not differ between foraging strategies and was unrelated to energy expenditure. Our findings suggest that energy expenditure in California sea lions may be influenced by interactions between diet and oxygen conservation strategies. There were no apparent energetic trade-offs between foraging strategies, although there was preliminary evidence that foraging strategies may differ in their variability in energy balance. The energetic consequences of behavioral variation may influence the reproductive success of female sea lions and result in differential impacts of individuals on prey populations. These findings highlight the importance of quantifying the relationships between energy expenditure and foraging behavior in other carnivores for studies addressing fundamental and applied physiological and ecological questions.

Prey fish returned to Forster's tern colonies suggest spatial and temporal differences in fish composition and availability.

Predators sample the available prey community when foraging; thus, changes in the environment may be reflected by changes in predator diet and foraging preferences. We examined Forster's tern (Sterna forsteri) prey species over an 11-year period by sampling approximately 10,000 prey fish returned to 17 breeding colonies in south San Francisco Bay, California. We compared the species composition among repeatedly-sampled colonies (≥ 4 years), using both relative species abundance and the composition of total dry mass by species. Overall, the relative abundances of prey species at seven repeatedly-sampled tern colonies were more different than would be expected by chance, with the most notable differences in relative abundance observed between geographically distant colonies. In general, Mississippi silverside (Menidia audens) and topsmelt silverside (Atherinops affinis) comprised 42% of individuals and 40% of dry fish mass over the study period. Three-spined stickleback (Gasterosteus aculeatus) comprised the next largest proportion of prey species by individuals (19%) but not by dry mass (6%). Five additional species each contributed ≥ 4% of total individuals collected over the study period: yellowfin goby (Acanthogobius flavimanus; 10%), longjaw mudsucker (Gillichthys mirabilis; 8%), Pacific herring (Clupea pallasii; 6%), northern anchovy (Engraulis mordax; 4%), and staghorn sculpin (Leptocottus armatus; 4%). At some colonies, the relative abundance and biomass of specific prey species changed over time. In general, the abundance and dry mass of silversides increased, whereas the abundance and dry mass of three-spined stickleback and longjaw mudsucker decreased. As central place foragers, Forster's terns are limited in the distance they forage; thus, changes in the prey species returned to Forster's tern colonies suggest that the relative availability of some fish species in the environment has changed, possibly in response to alteration of the available habitat.

Foraging and fasting can influence contaminant concentrations in animals: an example with mercury contamination in a free-ranging marine mammal.

Large fluctuations in animal body mass in relation to life-history events can influence contaminant concentrations and toxicological risk. We quantified mercury concentrations in adult northern elephant seals (Mirounga angustirostris) before and after lengthy at sea foraging trips (n = 89) or fasting periods on land (n = 27), and showed that mercury concentrations in blood and muscle changed in response to these events. The highest blood mercury concentrations were observed after the breeding fast, whereas the highest muscle mercury concentrations were observed when seals returned to land to moult. Mean female blood mercury concentrations decreased by 30% across each of the two annual foraging trips, demonstrating a foraging-associated dilution of mercury concentrations as seals gained mass. Blood mercury concentrations increased by 103% and 24% across the breeding and moulting fasts, respectively, demonstrating a fasting-associated concentration of mercury as seals lost mass. In contrast to blood, mercury concentrations in female's muscle increased by 19% during the post-breeding foraging trip and did not change during the post-moulting foraging trip. While fasting, female muscle mercury concentrations increased 26% during breeding, but decreased 14% during moulting. Consequently, regardless of exposure, an animal's contaminant concentration can be markedly influenced by their annual life-history events.

Oxygen minimum zone: An important oceanographic habitat for deep-diving northern elephant seals, Mirounga angustirostris.

Little is known about the foraging behavior of top predators in the deep mesopelagic ocean. Elephant seals dive to the deep biota-poor oxygen minimum zone (OMZ) (>800 m depth) despite high diving costs in terms of energy and time, but how they successfully forage in the OMZ remains largely unknown. Assessment of their feeding rate is the key to understanding their foraging behavior, but this has been challenging. Here, we assessed the feeding rate of 14 female northern elephant seals determined by jaw motion events (JME) and dive cycle time to examine how feeding rates varied with dive depth, particularly in the OMZ. We also obtained video footage from seal-mounted videos to understand their feeding in the OMZ. While the diel vertical migration pattern was apparent for most depths of the JME, some very deep dives, beyond the normal diel depth ranges, occurred episodically during daylight hours. The midmesopelagic zone was the main foraging zone for all seals. Larger seals tended to show smaller numbers of JME and lower feeding rates than smaller seals during migration, suggesting that larger seals tended to feed on larger prey to satisfy their metabolic needs. Larger seals also dived frequently to the deep OMZ, possibly because of a greater diving ability than smaller seals, suggesting their dependency on food in the deeper depth zones. Video observations showed that seals encountered the rarely reported ragfish (Icosteus aenigmaticus) in the depths of the OMZ, which failed to show an escape response from the seals, suggesting that low oxygen concentrations might reduce prey mobility. Less mobile prey in OMZ would enhance the efficiency of foraging in this zone, especially for large seals that can dive deeper and longer. We suggest that the OMZ plays an important role in structuring the mesopelagic ecosystem and for the survival and evolution of elephant seals.

A critical evaluation of the utility of eggshells for estimating mercury concentrations in avian eggs.

Eggshells are a potential tool for nonlethally sampling contaminant concentrations in bird eggs, yet few studies have examined their utility to represent mercury exposure. We assessed mercury concentrations in eggshell components for 23 bird species and determined whether they correlated with total mercury (THg) in egg contents. We designed a multi-experiment analysis to examine how THg is partitioned into eggshell components, specifically hardened eggshells, material adhered to the eggshells, and inner eggshell membranes. The THg concentrations in eggshells were much lower than in egg contents, and almost all of the THg within the eggshell was contained within material adhered to eggshells and inner eggshell membranes, and specifically not within calcium-rich hardened eggshells. Despite very little mercury in hardened eggshells, THg concentrations in hardened eggshells had the strongest correlation with egg contents among all eggshell components. However, species with the same THg concentrations in eggshells had different THg concentrations in egg contents, indicating that there is no global predictive equation among species for the relationship between eggshell and egg content THg concentrations. Furthermore, for all species, THg concentrations in eggshells decreased with relative embryo age. Although the majority of mercury in eggshells was contained within other eggshell components and not within hardened eggshells, THg in hardened eggshells can be used to estimate THg concentrations in egg contents, if embryo age and species are addressed. Environ Toxicol Chem 2017;36:2417-2427. Published 2017 Wiley Periodicals Inc. on behalf of SETAC. This article is a US government work and, as such, is in the public domain in the United States of America.