RESEARCH ARTICLE bark resistance in the , Antrozous pallidus

Bradley H. Hopp1, Ryan S. Arvidson2, Michael E. Adams1,2, Khaleel A. Razak1,3*

1 Graduate Neuroscience Program, University of , Riverside, California, United States of America, 2 Departments of Entomology and Cell Biology & Neuroscience, University of California, Riverside, California, United States of America, 3 Department of Psychology, University of California, Riverside, California, United States of America

* [email protected] a1111111111 a1111111111 a1111111111 Abstract a1111111111 a1111111111 The pallid bat (Antrozous pallidus), a gleaning bat found in the western United States and , hunts a wide variety of ground-dwelling prey, including . Anecdotal evi- dence suggests that the pallid bat is resistant to scorpion venom, but no systematic study has been performed. Here we show with behavioral measures and direct injection of venom that the pallid bat is resistant to venom of the , sculptura- OPEN ACCESS tus. Our results show that the pallid bat is stung multiple times during a hunt without any Citation: Hopp BH, Arvidson RS, Adams ME, noticeable effect on behavior. In addition, direct injection of venom at mouse LD50 concen- Razak KA (2017) Arizona bark scorpion venom resistance in the pallid bat, Antrozous pallidus. trations (1.5 mg/kg) has no effect on bat behavior. At the highest concentration tested (10 PLoS ONE 12(8): e0183215. https://doi.org/ mg/kg), three out of four bats showed no effects. One of the four bats showed a transient 10.1371/journal.pone.0183215 effect suggesting that additional studies are required to identify potential regional variation in Editor: Paulo Lee Ho, Instituto Butantan, BRAZIL venom tolerance. Scorpion venom is a cocktail of toxins, some of which activate voltage-

Received: December 1, 2016 gated sodium ion channels, causing intense pain. Dorsal root ganglia (DRG) contain noci- ceptive neurons and are principal targets of scorpion venom toxins. To understand if Accepted: August 1, 2017 mutations in specific ion channels contribute to venom resistance, a pallid bat DRG tran- Published: August 30, 2017 scriptome was generated. As sodium channels are a major target of scorpion venom, we Copyright: © 2017 Hopp et al. This is an open identified amino acid substitutions present in the pallid bat that may lead to venom resis- access article distributed under the terms of the tance. Some of these substitutions are similar to corresponding amino acids in sodium Creative Commons Attribution License, which permits unrestricted use, distribution, and channel isoforms responsible for reduced venom binding activity. The substitution found reproduction in any medium, provided the original previously in the providing venom resistance to the bark scorpion is not author and source are credited. present in the pallid bat, indicating a potentially novel mechanism for venom resistance in Data Availability Statement: All relevant data are the bat that remains to be identified. Taken together, these results indicate that the pallid bat included within the paper and its Supporting is resistant to venom of the bark scorpion and altered sodium ion channel function may Information files. The sequences for SCN10a partly underlie such resistance. (Nav1.8) and SCN9a (Nav1.7) have been deposited in GenBank Nav1.7 (GenBank Accession MF616470) and Nav1.8 (GenBank Accession MF616471).

Funding: This study was funded by the UC Riverside Academic Senate and Office of Research Introduction and Economic