Metal‐mediated climate susceptibility in a warming world: Larval and latent effects on a model amphibian

Abstract

Although sophisticated models predict the effects of future temperatures on ectotherms, few also address how ubiquitous sublethal contaminants alter an organism's response to thermal stress. In ectotherms, higher metabolic rates from warming temperatures can beneficially speed metabolism and development. If compounded by chronic, sublethal pollution, additional resource demands for elimination or detoxification may limit their ability to cope with rising temperatures-the toxicant-induced climate susceptibility hypothesis. In outdoor bioassays, using natural lake water as the background, the authors investigated the development of a model ectotherm in 6 levels of Cd, Cu, and Pb mixtures and 3 thermal regimes of diel temperature fluctuations: ambient, +1.5 °C, and +2.5 °C. Warming had no effect on wild-caught Cope's gray tree frog (Hyla chrysoscelis) until metals concentrations were approximately 10-fold of their bioavailable chronic criterion unit (sums of bioavailable fractions of chronic criteria concentrations). In treatments with ≥10 bioavailable chronic criterion units and +1.5 °C, growth increased. Conversely, in treatments with 28 bioavailable chronic criterion units and maximal +2.5 °C warming, growth declined and the body condition of postmetamorphic juveniles at 20 d was 34% lower than that of juveniles from background conditions (lake water at ambient temperatures). These findings suggest toxicant-induced climate susceptibility with long-term latent effects on the juvenile life stage. Sublethal contaminants can intensify the impact on aquatic ectotherms at the most conservative levels of predicted global warming over the next century. Environ Toxicol Chem 2016;35:1872-1882. © 2015 SETAC.

Strong Delayed Interactive Effects of Metal Exposure and Warming: Latitude-Dependent Synergisms Persist Across Metamorphosis

“…Despite the concern that trace metals become more toxic at higher temperatures , and the potential of strong delayed effects of metals during and after metamorphosis (see above), delayed interactive effects between metals and warming have been largely ignored. The only exception are two studies showing delayed sublethal effects of previous exposure to metals being magnified under warming (for adult body mass: ref , for juvenile body condition: ref ). Here, we showed that also across metamorphosis delayed effects of a metal can be magnified under warming, and even translated in a synergistic lethal effect by shortening adult lifespan.…”

“…This strong postmetamorphic lethal effect of zinc complements the very few documented adverse metal effects across metamorphosis: lowered survival in bryozoans, 14 lowered fecundity in mosquitoes, 60 lowered immune function and delayed reproduction in flies, 27 and reduced body condition in juvenile frogs. 28 Although some elimination of metals can happen during metamorphosis (e.g., via the shed larval skins), metal body burdens after metamorphosis can still remain very high. 61,62 Moreover, in addition to the stress that metamorphosis itself creates, the remobilization of stored metals during tissue reorganization at metamorphosis has been suggested to magnify the effects of metals.…”

“…In animals with a so-called complex life cycle, such delayed effects may be revealed or magnified at metamorphosis, which has been identified as a sensitive, stressful event (“stressful metamorphosis hypothesis”) . This is because the process of metamorphosis involves substantial tissue construction and reorganization, and requires a considerable amount of energy. , Recent studies demonstrated severe lethal effects of contaminants in aquatic insects during metamorphosis despite the absence of any effects during the preceding larval exposure period. − Yet, also after successful metamorphosis, there is still potential for delayed effects. ,, While studies are more frequently considering such delayed effects of single stressors across metamorphosis, and despite the increasing concern that interactions between stressors also occur when they are encountered sequentially, , delayed postmetamorphic effects of combined larval exposure to contaminants and other stressors, particularly warming, are very limited (but see refs , ). Understanding how aquatic stressors affect aquatic insect emergence and their postmetamorphic survival is important for managing both aquatic and riparian ecosystems as aquatic insects subsidize the diets of terrestrial insectivores such as spiders and birds. , …”

Extreme Arsenic and Antimony Uptake and Tolerance in Toad Tadpoles during Development in Highly Contaminated Wetlands

“…Arsenic and antimony concentrations in water, sediment, primary producers, and tadpoles at sites HS, CP, and OP were previously quantified; detailed descriptions of methods and results were provided in 2016 in the work of Dovick et al 12 For the present study, we quantified As and Sb concentrations in water and sediment samples collected during the middle of our sampling schedule (day 185), using the protocol described in the Dovick et al work 12 and in tadpole samples collected on each site visit using protocols described below. To account for the known effects of water temperature on tadpole growth and development, 14 including interactions with contaminants, 15 we deployed a water temperature data logger (32K StowAway Tidbit −5 °C to 37 °C logger, Onset Computer Corp., Bourne, MA, USA) in each site at a shoreline used by tadpoles. We placed a solar radiation shield over each logger to prevent direct sunlight from reaching the device through the shallow (ca.…”

Combined effects of cadmium exposure and temperature on the annual killifish (Nothobranchius furzeri)

“…Organisms in polluted environments are typically exposed to a cocktail of stressors. Trace metals are, for instance, omnipresent in freshwater ecosystems; and combined with the effects of global warming they can be harmful at low concentrations to aquatic organisms including fish (Noyes and Lema 2015), amphibians (Hallman and Brooks 2016), and insects such as damselflies (Debecker et al 2017). This is attributable to the fact that environmental warming increases the body temperature of ectothermic animals and will alter physiological and biochemical reactions but also will affect the stability of biological molecules (Sokolova and Lannig 2008).…”