Effects of sublethal methylmercury and food stress on songbird energetic performance: metabolic rates, molt and feather quality.

Organisms regularly adjust their physiology and energy balance in response to predictable seasonal environmental changes. Stressors and contaminants have the potential to disrupt these critical seasonal transitions. No studies have investigated how simultaneous exposure to the ubiquitous toxin methylmercury (MeHg) and food stress affects birds' physiological performance across seasons. We quantified several aspects of energetic performance in song sparrows, Melospiza melodia, exposed or not to unpredictable food stress and MeHg in a 2×2 experimental design, over 3 months during the breeding season, followed by 3 months post-exposure. Birds exposed to food stress had reduced basal metabolic rate and non-significant higher factorial metabolic scope during the exposure period, and had a greater increase in lean mass throughout most of the experimental period. Birds exposed to MeHg had increased molt duration, and increased mass:length ratio of some of their primary feathers. Birds exposed to the combined food stress and MeHg treatment often had responses similar to the stress-only or MeHg-only exposure groups, suggesting these treatments affected physiological performance through different mechanisms and resulted in compensatory or independent effects. Because the MeHg and stress variables were selected in candidate models with a ΔAICc lower than 2 but the 95% confidence interval of these variables overlapped zero, we found weak support for MeHg effects on all measures except basal metabolic rate, and for food stress effects on maximum metabolic rate, factorial metabolic scope and feather mass:length ratio. This suggests that MeHg and food stress effects on these measures are statistically identified but not simple and/or were too weak to be detected via linear regression. Overall, combined exposure to ecologically relevant MeHg and unpredictable food stress during the breeding season does not appear to induce extra energetic costs for songbirds in the post-exposure period. However, MeHg effects on molt duration could carry over across multiple annual cycle stages.

Methylmercury effects on avian brains.

Methylmercury (MeHg) is a concerning contaminant due to its ubiquity and harmful effects on organisms. Although birds are important models in the neurobiology of vocal learning and adult neuroplasticity, the neurotoxic effects of MeHg are less understood in birds than mammals. We surveyed the literature on MeHg effects on biochemical changes in the avian brain. Publication rates of papers related to neurology and/or birds and/or MeHg increased with time and can be linked with historical events, regulations, and increased understanding of MeHg cycling in the environment. However, publications on MeHg effects on the avian brain remain relatively low across time. The neural effects measured to evaluate MeHg neurotoxicity in birds changed with time and researcher interest. The measures most consistently affected by MeHg exposure in birds were markers of oxidative stress. NMDA, acetylcholinesterase, and Purkinje cells also seem sensitive to some extent. MeHg exposure has the potential to affect most neurotransmitter systems but more studies are needed for validation in birds. We also review the main mechanisms of MeHg-induced neurotoxicity in mammals and compare it to what is known in birds. The literature on MeHg effects on the avian brain is limited, preventing full construction of an adverse outcome pathway. We identify research gaps for taxonomic groups such as songbirds, and age- and life-stage groups such as immature fledgling stage and adult non-reproductive life stage. In addition, results are often inconsistent between experimental and field studies. We conclude that future neurotoxicological studies of MeHg impacts on birds need to better connect the numerous aspects of exposure from molecular physiological effects to behavioural outcomes that would be ecologically or biologically relevant for birds, especially under challenging conditions.

Effects of methylmercury and food stress on migratory activity in song sparrows, Melospiza melodia.

Avian migration is a challenging life stage susceptible to the adverse effects of stressors, including contaminants like methylmercury (MeHg). Although birds often experience stressors and contaminants concurrently in the wild, no study to date has investigated how simultaneous exposure to MeHg and food stress affects migratory behavior. Our objectives were to determine if MeHg or food stress exposure during summer, alone or combined, has carry-over effects on autumn migratory activity, and if hormone levels (corticosterone, thyroxine) and body condition were related to these effects. We tested how exposure to dietary MeHg and/or food stress (unpredictable temporary food removal) affected migratory behavior in captive song sparrows, Melospiza melodia. Nocturnal activity was influenced by a 3-way interaction between MeHg × stress × nights of the study, indicating that activity changed over time in different ways depending on prior treatments. Thyroxine was not affected by treatment or sampling date. During the migratory season, fecal corticosterone metabolite concentrations increased in birds co-exposed to MeHg and food stress compared to controls, suggesting an additive carry-over effect. As well, during the period of behavioral recording, body condition increased with time in unstressed birds, but not in stressed birds. Fecal corticosterone metabolite concentrations were positively correlated to duration of nocturnal activity, but thyroxine levels and body condition were not. The differences in nocturnal activity between groups suggest that food stress and MeHg exposure on breeding grounds could have direct and indirect carry-over effects that have the potential to affect the fall migration journey.

Neurogenesis and the development of neural sex differences in vocal control regions of songbirds.

The brain regions that control the learning and production of song and other learned vocalizations in songbirds exhibit some of the largest sex differences in the brain known in vertebrates and are associated with sex differences in singing behavior. Song learning takes place through multiple stages: an early sensory phase when song models are memorized, followed by a sensorimotor phase in which auditory feedback is used to modify song output through subsong, plastic song, to adult crystalized song. However, how patterns of neurogenesis in these brain regions change through these learning stages, and differ between the sexes, is little explored. We collected brains from 63 young male and female zebra finches (Taeniopygia guttata) over four stages of song learning. Using neurogenesis markers for cell division (proliferating cell nuclear antigen), neuron migration (doublecortin), and mature neurons (neuron-specific nuclear protein), we demonstrate that there are sex-specific changes in neurogenesis over song development that differ between the caudal motor pathway and anterior forebrain pathway of the vocal control circuit. In many of these regions, sex differences emerged very early in development, by 25 days post hatch, at the beginning of song learning. The emergence of sex differences in other components of the system was more gradual and had specific trajectories depending on the brain region and its function. In conclusion, we found that sex differences occurred early and continued during song learning. Moreover, transitions from the different phases of song development do not seem to depend on large changes in neurogenesis in the vocal control areas measured.

Feathers accurately reflect blood mercury at time of feather growth in a songbird.

Methylmercury (MeHg) is a globally distributed pollutant that can negatively affect wildlife. Bird feathers are often used as a monitoring tool of contaminant exposure, but variability in total mercury (THg) content in flight feathers has raised concerns over their utility. The objective of this study was to quantify blood and feather THg depuration through the progression of primary feather molt in order to clarify the relationship between blood and feather mercury concentration, and test the reliability of feather THg measurements as a monitoring tool in wild songbirds. Song sparrows (Melospiza melodia) were experimentally exposed to dietary MeHg and their blood and primary feather THg concentrations were measured during exposure and post-exposure periods of three months each. A rapid decrease in feather and blood THg concentration through molt progression was observed. Primary feather THg content was higher in feathers grown during the MeHg exposure period compared to those grown during the post-exposure period. Primary feather THg concentration was highly correlated with blood THg measured at the time of feather growth (R = 0.98), indicating that, although THg concentration is variable among flight feathers, this reflects temporally sequential molting patterns and declining blood concentration during depuration. Primary flight feathers thus provide an accurate and useful tool for estimating the mercury burden of birds at the time a chosen feather was grown, and have the potential to be an effective and reliable biomonitoring tool for species with well-characterized molt patterns.