Anthropogenic Zinc Exposure Increases Mortality and Antioxidant Gene Expression in Monarch Butterflies with Low Access to Dietary Macronutrients

Alexander M. Shephard, Noah S. Brown, Emilie C. Snell-Rood

Research output: Contribution to journalComment/debatepeer-review

Abstract

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.

Original languageEnglish (US)
Pages (from-to)1286-1296
Number of pages11
JournalEnvironmental Toxicology and Chemistry
Volume41
Issue number5
DOIs
StatePublished - May 2022

Bibliographical note

Funding Information:
The present study was supported by the Minnesota Environment and Natural Resources Trust Fund as recommended by the Legislative-Citizen Commission on Minnesota Resources. Funding was also provided by a Bell Museum Natural History Award from the Dayton Fund and an Ecology, Evolution, and Behavior Summer Research Award from the University of Minnesota. We thank L. Hagg and A. Stene for helping to start and maintain the monarch rearing population for our study. We also thank C. Taylor and his research group at the University of Kansas for providing the monarch semi-artificial diet. Element analysis was performed at the Northwestern University Quantitative Bio-element Imaging Center generously supported by the National Aeronautics and Space Ames Research Center (Grant NNA04CC36G).

Funding Information:
The present study was supported by the Minnesota Environment and Natural Resources Trust Fund as recommended by the Legislative‐Citizen Commission on Minnesota Resources. Funding was also provided by a Bell Museum Natural History Award from the Dayton Fund and an Ecology, Evolution, and Behavior Summer Research Award from the University of Minnesota. We thank L. Hagg and A. Stene for helping to start and maintain the monarch rearing population for our study. We also thank C. Taylor and his research group at the University of Kansas for providing the monarch semi‐artificial diet. Element analysis was performed at the Northwestern University Quantitative Bio‐element Imaging Center generously supported by the National Aeronautics and Space Ames Research Center (Grant NNA04CC36G).

Publisher Copyright:
© 2022 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC

Keywords

  • Antioxidant
  • Heavy metal
  • Macronutrient
  • Monarch butterfly
  • Nutritional ecology
  • Oxidative stress
  • Zinc

PubMed: MeSH publication types

  • Journal Article
  • Research Support, Non-U.S. Gov't

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