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Research Article

Anthropogenic changes in sodium affect neural and muscle development in butterflies

Emilie C. Snell-Rood, Anne Espeset, Christopher J. Boser, William A. White, and Rhea Smykalski
  1. aDepartment of Ecology, Evolution and Behavior, University of Minnesota, St. Paul, MN 55108; and
  2. bDepartment of Biology, University of Nevada, Reno, NV 89557-0314

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PNAS first published June 9, 2014; https://doi.org/10.1073/pnas.1323607111
Emilie C. Snell-Rood
aDepartment of Ecology, Evolution and Behavior, University of Minnesota, St. Paul, MN 55108; and
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  • For correspondence: emilies@umn.edu
Anne Espeset
aDepartment of Ecology, Evolution and Behavior, University of Minnesota, St. Paul, MN 55108; and
bDepartment of Biology, University of Nevada, Reno, NV 89557-0314
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Christopher J. Boser
aDepartment of Ecology, Evolution and Behavior, University of Minnesota, St. Paul, MN 55108; and
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William A. White
aDepartment of Ecology, Evolution and Behavior, University of Minnesota, St. Paul, MN 55108; and
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Rhea Smykalski
aDepartment of Ecology, Evolution and Behavior, University of Minnesota, St. Paul, MN 55108; and
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  1. Edited by May R. Berenbaum, University of Illinois at Urbana–Champaign, Urbana, IL, and approved May 6, 2014 (received for review December 28, 2013)

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Significance

Sodium is an essential micronutrient that is often limited in animal diets. It is important in the development of neural tissue and thought to have driven the evolution of specific foraging behavior. Human activity is drastically altering patterns of sodium availability, particularly through road salt application, but we know little about the consequences of such anthropogenic change on the development and evolution of wild animals. Here, we show that road salt runoff affects sodium concentrations of roadside plants, which in turn, have significant, (sometimes positive) effects on neural and muscular development of herbivores. These results suggest that anthropogenic changes in sodium can have major consequences for both behavioral development and selection on foraging behavior.

Abstract

The development of organisms is changing drastically because of anthropogenic changes in once-limited nutrients. Although the importance of changing macronutrients, such as nitrogen and phosphorus, is well-established, it is less clear how anthropogenic changes in micronutrients will affect organismal development, potentially changing dynamics of selection. We use butterflies as a study system to test whether changes in sodium availability due to road salt runoff have significant effects on the development of sodium-limited traits, such as neural and muscle tissue. We first document how road salt runoff can elevate sodium concentrations in the tissue of some plant groups by 1.5–30 times. Using monarch butterflies reared on roadside- and prairie-collected milkweed, we then show that road salt runoff can result in increased muscle mass (in males) and neural investment (in females). Finally, we use an artificial diet manipulation in cabbage white butterflies to show that variation in sodium chloride per se positively affects male flight muscle and female brain size. Variation in sodium not only has different effects depending on sex, but also can have opposing effects on the same tissue: across both species, males increase investment in flight muscle with increasing sodium, whereas females show the opposite pattern. Taken together, our results show that anthropogenic changes in sodium availability can affect the development of traits in roadside-feeding herbivores. This research suggests that changing micronutrient availability could alter selection on foraging behavior for some roadside-developing invertebrates.

  • nutritional ecology
  • Danaus plexippus
  • Pieris rapae
  • ecological stoichiometry

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: emilies{at}umn.edu.
  • Author contributions: E.C.S.-R. and A.E. designed research; E.C.S.-R., A.E., W.A.W., and R.S. performed research; E.C.S.-R. analyzed data; and E.C.S.-R. and C.J.B. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The data reported in this paper have been deposited in the DRYAD database, http://datadryad.org (doi:10.5061/dryad.v2t58).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1323607111/-/DCSupplemental.

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Salt runoff affects herbivore development
Emilie C. Snell-Rood, Anne Espeset, Christopher J. Boser, William A. White, Rhea Smykalski
Proceedings of the National Academy of Sciences Jun 2014, 201323607; DOI: 10.1073/pnas.1323607111

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Salt runoff affects herbivore development
Emilie C. Snell-Rood, Anne Espeset, Christopher J. Boser, William A. White, Rhea Smykalski
Proceedings of the National Academy of Sciences Jun 2014, 201323607; DOI: 10.1073/pnas.1323607111
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    - Jun 25, 2014
Proceedings of the National Academy of Sciences: 118 (14)
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