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Monarch caterpillars are robust to combined exposure to the roadside micronutrients sodium and zinc.

ABSTRACT: Human activities are increasing the environmental availability of micronutrients, including sodium and some essential metals. Micronutrients are often limiting in animal diets but may have negative effects when consumed in excess. Though prior research has documented how elevated exposure to individual micronutrients can impact organismal development and fitness, we know less about combined effects of multiple micronutrients. In the wild, monarch butterfly larvae (Danaus plexippus) commonly consume plants in roadside habitats that contain elevated levels of sodium (from road salt) and zinc (from vehicle wear-and-tear). We reared monarch caterpillars to adulthood to test individual and combined effects of dietary sodium and zinc on components of fitness, sodium-linked phenotypes (proxies for neural and flight muscle development) and concentrations of sodium and zinc in adult butterflies. Monarch survival was not impacted by elevated sodium or zinc individually or in combination. Yet, monarchs feeding on sodium-treated milkweed developed relatively larger eyes, consistent with a positive effect of sodium on neural development. Measurements of element concentrations in butterfly and plant tissue indicated that monarchs had higher zinc levels than those present in zinc-treated milkweed but lower sodium levels than those present in sodium-treated milkweed. Monarchs developing on sodium-treated milkweed also had prolonged development time, which might be a cost associated with developing extra neural tissue or investing in mechanisms to excrete excess dietary sodium during the larval stage. Our results indicate that sodium, more than zinc, is likely influencing phenotypic development and performance of insect pollinators in roadside habitats. Yet, in contrast to previous work, our experiment suggests that the highest levels of sodium found along roads are not always harmful for developing monarchs. Future work could consider how potentially stressful effects of micronutrients could be mitigated by increased macronutrient availability or how developmental factors such as migratory status might increase micronutrient requirements.

SUBMITTER: Shephard AM

PROVIDER: S-EPMC8354372 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Biologists seek to understand why organisms vary in their abilities to tolerate anthropogenic contaminants, such as heavy metals. However, few studies have considered how tolerance may be affected by condition-moderating factors such as dietary resource availability. For instance, the availability of crucial limiting macronutrients, such as nitrogen and phosphorous, can vary across space and time either naturally or due to anthropogenic nutrient inputs (e.g., agricultural fertilizers or vehicle emissions). Organisms developing in more macronutrient-rich environments should be of higher overall condition, displaying a greater ability to tolerate metal contaminants. In monarch butterflies (Danaus plexippus), we factorially manipulated dietary macronutrient availability and exposure to zinc, a common metal contaminant in urban habitats that can be toxic but also has nutritional properties. We tested whether (1) the ability to survive zinc exposure depends on dietary macronutrient availability and (2) whether individuals exposed to elevated zinc levels display higher expression of antioxidant genes, given the roles of antioxidants in combatting metal-induced oxidative stress. Exposure to elevated zinc reduced survival only for monarchs developing on a low-macronutrient diet. However, for monarchs developing on a high-macronutrient diet, elevated zinc exposure tended to increase survival. In addition, monarchs exposed to elevated zinc displayed higher expression of antioxidant genes when developing on the low-macronutrient diet but lower expression when developing on the high-macronutrient diet. Altogether, our study shows that organismal survival and oxidative stress responses to anthropogenic zinc contamination depend on the availability of macronutrient resources in the developmental environment. In addition, our results suggest the hypothesis that whether zinc acts as a toxicant or a nutrient may depend on macronutrient supply. Environ Toxicol Chem 2022;41:1286-1296. © 2022 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

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Monarch caterpillars are robust to combined exposure to the roadside micronutrients sodium and zinc.

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