Complex Life Histories Alter Patterns of Mercury Exposure and Accumulation in a Pond-Breeding Amphibian

Abstract

Quantifying how contaminants change across life cycles of species that undergo metamorphosis is critical to assessing organismal risk, particularly for consumers. Pond-breeding amphibians can dominate aquatic animal biomass as larvae and are terrestrial prey as juveniles and adults. Thus, amphibians can be vectors of mercury exposure in both aquatic and terrestrial food webs. However, it is still unclear how mercury concentrations are affected by exogenous (e.g., habitat or diet) vs endogenous factors (e.g., catabolism during hibernation) as amphibians undergo large diet shifts and periods of fasting during ontogeny. We measured total mercury (THg), methylmercury (MeHg), and isotopic compositions (δ 13 C, δ 15 N) in boreal chorus frogs (Pseudacris maculata) across five life stages in two Colorado (USA) metapopulations. We found large differences in concentrations and percent MeHg (of THg) among life stages. Frog MeHg concentrations peaked during metamorphosis and hibernation coinciding with the most energetically demanding life cycle stages. Indeed, life history transitions involving periods of fasting coupled with high metabolic demands led to large increases in mercury concentrations. The endogenous processes of metamorphosis and hibernation resulted in MeHg bioamplification, thus decoupling it from the light isotopic proxies of diet and trophic position. These step changes are not often considered in conventional expectations of how MeHg concentrations within organisms are assessed.

Framework for multi-stressor physiological response evaluation in amphibian risk assessment and conservation

“…Distinguishing stagespecific endogenous variation in physiological processes enables anticipation of compromised physical condition in response to common stressors (Brooks and Kindsvater, 2022;Nolan et al, 2023). Here we focus on stressor impacts on transition between life (Denver, 2009;Duarte-Guterman et al, 2014;Thambirajah et al, 2019) GC ↑ to some xenobiotics (Burraco and Gomez-Mestre, 2016;Trudeau et al, 2020), environmental conditions (Sachs and Buchholz, 2019;Thambirajah et al, 2019), predators (Narayan et al, 2013) ; neurogenerative, oxidative, mitochondrial, teratological effects (Di Lorenzo et al, 2020) CS and TH levels in tissue or immersed water (Gabor et al, 2013a); tissue/ organism enzyme activity or DGE in AR, TR, tra, trb, dio2, dio3 (Thambirajah et al, 2022); ambient water assay; size at metamorphosis (Rowland et al, 2023); vitellogenin indicative of feminization (Venturino and de D'Angelo, 2005) Time to metamorphosis; cohort sex ratio; carryover to juvenile immunity, survival, fecundity (Kiesecker, 2002, Denver, 2009Kohli et al, 2019;Ruthsatz et al, 2020;Le Sage et al, 2022) Immunity Endocrine-driven development of immunity; immunosuppression at metamorphosis (Rollins-Smith, 2017)…”

Broad-Scale Assessment of Methylmercury in Adult Amphibians

“…Elevated MeHg exposure can also occur in other aquatic-dependent species, such as amphibians, ,, which can result in effects such as reduced hatching success via egg infertility and embryonic mortality . However, in comparison to other aquatic-dependent species, relatively little is still known about the variability in MeHg bioaccumulation for most amphibians, which limits understanding of the toxicological effects and potential population-level threats from MeHg. , …”

“…Methylmercury may pose unique risks to amphibians because amphibians depend on aquatic environments associated with elevated MeHg production for key periods of their life history. Physiologically stressful events like metamorphosis and hibernation can also remobilize stored MeHg, redistribute tissue concentrations, and ultimately influence susceptibility to stressors, including emergent infectious diseases . Also, because many amphibians rely on aquatic and terrestrial environments, they can serve as MeHg vectors to both aquatic and terrestrial predators. , Despite the potential threats that MeHg poses to amphibians, geographic variation in the magnitude, distribution, and variability of MeHg bioaccumulation among populations is not well documented in comparison to other taxa such as fishes and invertebrates. , Most research on amphibian MeHg has focused on the aquatic, larval life stage rather than adults (but see refs − ), despite adults generally occupying higher trophic positions and whose survival typically has a greater effect on population trajectories compared to larvae (e.g., refs and ).…”

“…14 However, in comparison to other aquatic-dependent species, relatively little is still known about the variability in MeHg bioaccumulation for most amphibians, which limits understanding of the toxicological effects and potential population-level threats from MeHg. 13,15 Methylmercury may pose unique risks to amphibians because amphibians depend on aquatic environments associated with elevated MeHg production for key periods of their life history. Physiologically stressful events like metamorphosis and hibernation can also remobilize stored MeHg, redistribute tissue concentrations, and ultimately influence susceptibility to stressors, including emergent infectious diseases.…”

“…Physiologically stressful events like metamorphosis and hibernation can also remobilize stored MeHg, redistribute tissue concentrations, and ultimately influence susceptibility to stressors, including emergent infectious diseases. 15 Also, because many amphibians rely on aquatic and terrestrial environments, they can serve as MeHg vectors to both aquatic and terrestrial predators. 16,17 Despite the potential threats that MeHg poses to amphibians, geographic variation in the magnitude, distribution, and variability of MeHg bioaccumulation among populations is not well documented in comparison to other taxa such as fishes and invertebrates.…”