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Defensive alkaloid variation and palatability in sympatric poison frogs

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Abstract

Chemical defense in poison frogs derives from lipophilic alkaloids sequestered from dietary arthropods. Alkaloid composition varies extensively among individuals, populations, and species. Numerous causes of intraspecific variation have been identified, but the causes of interspecific variation are less clear, with both intrinsic (e.g., mechanism of sequestration) and extrinsic (e.g., arthropod availability) explanations being possible. Sympatric species afford a unique opportunity to investigate the causes and consequences of interspecific variation in natural populations, since they are potentially exposed to the same arthropod prey and predators. We used gas chromatography–mass spectrometry to identify alkaloids from 36 individuals of six species and three genera of dendrobatid poison frogs (Adelphobates, Ameerega, and Ranitomeya) collected in three Amazonian localities. We then compared alkaloid composition, richness, and quantity among sympatric species and analyzed the variation in alkaloid composition among con- and heterospecific populations at the two nearest localities. We also performed arthropod palatability experiments to investigate the biological significance of differences in alkaloids among sympatric species. Sympatric species differed in alkaloid composition, richness, and quantity, and conspecific individuals from different localities shared more alkaloids than heterospecific individuals from the same locality, strongly suggesting that variation is due to intrinsic causes. All analyzed alkaloid secretions were unpalatable, but palatability scores did not differ for most sympatric species, despite significant differences in alkaloid composition, richness, and quantity. Our results provide insights into the causes and consequences of interspecific variation in alkaloid profiles, but additional data are required to identify specific intrinsic causes and predator responses.

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Data availability

All data supporting the findings of this study are included within the paper and its Supplementary materials, including Supplementary material 1. Alklaloid richness and quantity and skin mass for the 36 individual poison frogs examined in the present study; Supplementary material 2. Differences in alkaloid richness and quantity among sympatric poison frogs, estimated with pairwise comparisons after Bonferroni correction using GLMs; and Supplementary material 3. Pairwise differences in palatability between sympatric poison frogs in Locality 1.

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Acknowledgements

P. Colombo, D.A.F. Grant, D.B. Miranda, V.G.D. Orrico, and C. Zank provided assistance during fieldwork in Acre, and S. Andrade, C.A. Lopes, J. Ospina-Sarria, M. Rada, the São Sebastião and Vila do Bravo communities, and the crew of Estação Científica Ferreira Penna (Museu Paraense Emílio Goeldi, Universidade Federal do Pará) provided logistical support and assistance during fieldwork in Pará. We thank M. Nichols for his assistance in maintaining the GC–MS at JCU.

Funding

This research was supported by the Brazilian Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq Proc. 306823/2017-9, 311509/2020-7, 314480/2021-8), Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP Proc. 2012/10000-5, 2016/09999-9, 2018/15425-0, 2021/14522-5, 2022/07325-1), Kresge Foundation, and Colleran-Weaver.

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Authors

Contributions

AMJ, JAP, RAS, and TG contributed to study conception and design. AMJ, PSB, and TG collected specimens. AMJ, JAP, and RAS performed chemical analyses. RAS and SK performed palatability tests. DYMN ad JAP performed statistical analyses. JAP wrote the first draft of the manuscript, which was then modified and approved by all authors.

Corresponding author

Correspondence to Taran Grant.

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Conflict of interest

The authors declare that they have no conflict of interest.

Permits

Collection permits were issued by the Brazilian Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio 12178-2, 54640-1, 13173-2), and authorization to export samples from Brazil to the USA was issued by the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA 17BR025049/DF).

Additional information

Communicated by Günther Raspotnig.

Supplementary Information

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Albuquerque-Pinna, J., Jeckel, A.M., Nakamura, D.Y.M. et al. Defensive alkaloid variation and palatability in sympatric poison frogs. Chemoecology (2024). https://doi.org/10.1007/s00049-024-00402-9

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  • DOI: https://doi.org/10.1007/s00049-024-00402-9

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