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Fortune favors the bold toad: urban-derived behavioral traits may provide advantages for invasive amphibian populations

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Abstract

Many biological invasions occur within and between urban areas. If native species adapted to anthropogenically altered habitats are subsequently moved from an urban area in their native range to one within a novel region, then their urban-specialized phenotypes may provide them an advantage via prior adaptation. Here we examine if urban-derived behavioral traits are present within native guttural toad, Sclerophrys gutturalis, populations (Durban, South Africa) and investigate whether these localized phenotypes persisted within their invasive populations in Mauritius and Réunion. In our study, we measured boldness and exploration in populations along the toad’s invasion route and found that toads were significantly bolder in urban populations, within both native and invasive ranges. This suggests boldness increased when toads transitioned to urban living in their native range and these heightened levels of boldness were maintained within invaded urban areas. This provides evidence that a bolder phenotype was a prior adaptation that likely increased guttural toad’s invasion success. Interestingly, toad boldness returned to pre-urbanization levels within invasive populations that spread into natural areas, replicated on both islands. Exploration, on the other hand, was not increased above pre-urbanization, or pre-invasion, levels for any of the populations, and was lower in toads from Mauritius. Overall, our findings suggest that increased boldness is favored in urban habitats and that urban-derived behavioral traits may provide individuals an advantage when invading new urban landscapes.

Significance statement

Species adapting to anthropogenic landscapes have the ability to increase their invasive potential if the altered phenotypes they accrue can provide them advantages once they are transported outside their native range. Our study examined differences in behavioral traits, boldness, and exploration, along the invasion route of guttural toads, Sclerophrys gutturalis, between natural and urban sites from their native origin populations around Durban, South Africa, to their invasive populations in Mauritius and Réunion. We determined that populations were bolder in urban areas in their native range and that this increased boldness persisted in the other anthropogenic habitats within their invasive ranges, but reverted back to natural-native levels within populations that had spread into natural areas on both islands. Our findings support the growing trend that anthropogenically altered landscapes favor bolder individuals, as well as the assertion that urban-derived traits may bolster a species’ ability to establish and spread within novel landscapes.

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Data availability

The datasets and R code for this study are available from Open Source Framework (OSF, DOI: https://doi.org/10.17605/OSF.IO/54TAC), which can be found here: https://osf.io/54tac/

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Acknowledgements

We would like to thank C. Baider, M. Campbell, A. Cheke, V. Florens, P. Kowalski, N. Mohanty, M. Mühlenhaupt, S. Peta, S. Sauroy-Toucouère, D. Strasberg, C. Wagener, and R. Wedderburn for their invaluable support and insights. We would also like to thank Black River Gorges National Park, the Durban Botanical Gardens, and the communities of Notre Dame, Villèle, and Pont Payet, and the anonymous reviewers whose comments improved this manuscript.

Funding

This work was supported by the DSI-NRF Centre of Excellence for Invasion Biology (JB-G & JM), the Centre for Collaborations in Africa at Stellenbosch University (JB-G), Claude Leon Foundation (fellowship to JLR), and the Natural Sciences and Engineering Research Council of Canada (fellowship to JLR).

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Correspondence to James Baxter-Gilbert or Julia L. Riley.

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Ethics approval

Ethical approval for toad captures and our experimental protocols followed animal ethics guidelines set out and approved by the Stellenbosch University’s Research Ethics Committee (Animal Care and Use: ACU-2020–10386). National guidelines for the use of animals in scientific research were followed (South Africa National Standard: The Care and Use of Animals for Scientific Purposes; SANS 20386:2008). This work was conducted with authorization from Ezemvelo KwaZulu-Natal Wildlife (Ordinary Permit: OP 4072/2019) and Mauritian National Parks and Conservation Services (NP 46/3 V3).

Conflict of interest

The authors declare no competing interests.

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Communicated by C. R Gabor

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James Baxter-Gilbert and Julia L. Riley have joint first authorship.

This article is a contribution to the Topical Collection Using behavioral ecology to explore adaptive responses to anthropogenic change – Guest Editors: Jan Lindström, Constantino Macias Garcia, Caitlin Gabor

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Baxter-Gilbert, J., Riley, J.L. & Measey, J. Fortune favors the bold toad: urban-derived behavioral traits may provide advantages for invasive amphibian populations. Behav Ecol Sociobiol 75, 130 (2021). https://doi.org/10.1007/s00265-021-03061-w

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  • DOI: https://doi.org/10.1007/s00265-021-03061-w

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