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Exposure to sublethal concentrations of a pesticide or predator cues induces changes in brain architecture in larval amphibians

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Abstract

Naturally occurring environmental factors shape developmental trajectories to produce variable phenotypes. Such developmental phenotypic plasticity can have important effects on fitness, and has been demonstrated for numerous behavioral and morphological traits. However, surprisingly few studies have examined developmental plasticity of the nervous system in response to naturally occurring environmental variation, despite accumulating evidence for neuroplasticity in a variety of organisms. Here, we asked whether the brain is developmentally plastic by exposing larval amphibians to natural and anthropogenic factors. Leopard frog tadpoles were exposed to predator cues, reduced food availability, or sublethal concentrations of the pesticide chlorpyrifos in semi-natural enclosures. Mass, growth, survival, activity, larval period, external morphology, brain mass, and brain morphology were measured in tadpoles and after metamorphosis. Tadpoles in the experimental treatments had lower masses than controls, although developmental rates and survival were similar. Tadpoles exposed to predator cues or a high dose of chlorpyrifos had altered body shapes compared to controls. In addition, brains from tadpoles exposed to predator cues or a low dose of chlorpyrifos were narrower and shorter in several dimensions compared to control tadpoles and tadpoles with low food availability. Interestingly, the changes in brain morphology present at the tadpole stage did not persist in the metamorphs. Our results show that brain morphology is a developmentally plastic trait that is responsive to ecologically relevant natural and anthropogenic factors. Whether these effects on brain morphology are linked to performance or fitness is unknown.

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Acknowledgments

We thank R.J. Bendis and Devin Jones for assistance in the field. This research was supported by Duquesne University (SKW) and NSF grant 11-19430 (RAR).

Author contribution statement

SKW and RAR formulated the idea. All authors designed the experiments. BMM, EKY, and RAR executed the experiments. BMM, EKY, and SKW collected data. SKW and RAR analyzed the data. All authors contributed to the writing of the manuscript. RAR and SKW funded the work.

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Authors and Affiliations

  1. Department of Biological Sciences, Duquesne University, Pittsburgh, PA, 15282, USA

    Sarah K. Woodley

  2. Department of Biological Sciences, Rensselaer Polytechnic Institute, Troy, NY, 12180, USA

    Brian M. Mattes & Rick A. Relyea

  3. Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, 15260, USA

    Erika K. Yates

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  1. Sarah K. Woodley
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  2. Brian M. Mattes
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Correspondence to Sarah K. Woodley.

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Communicated by Pieter Johnson.

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Woodley, S.K., Mattes, B.M., Yates, E.K. et al. Exposure to sublethal concentrations of a pesticide or predator cues induces changes in brain architecture in larval amphibians. Oecologia 179, 655–665 (2015). https://doi.org/10.1007/s00442-015-3386-3

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