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Are threatened seabird colonies of the pacific ocean genetically vulnerable? The case of the red-tailed tropicbird, Phaethon rubricauda, as a model species

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Abstract

Oceanic seabirds have suffered population declines and extirpations due to human disturbance and still face multiple threats. Here, we assessed the potential genetic vulnerability of the red-tailed tropicbird, Phaethon rubricauda, a seabird species threatened by human disturbance and listed as ‘least concern’ by the IUCN. Using Single Nucleotide Polymorphisms (SNPs) we evaluated the genetic population structure of the red-tailed tropicbird throughout the Pacific Ocean using samples from 132 individuals from six islands. We sampled individuals from islands without human-related disturbance (non-impacted islands) and with human-related disturbance (impacted islands). Results of genome-wide SNP analyses were consistent with previous results using mitochondrial DNA sequences analyses. Genetic diversity did not differ between impacted and non-impacted islands, and low inbreeding estimates were detected for all colonies. The SNPs analyses confirmed a pattern of isolation by distance and significant inter-regional (Chile, Australasia, and Hawaiʻi) genetic structure, but revealed greater differentiation of tropicbirds in Hawaiʻi compared with Chile and Australasia. Within regions, our results further indicated significant differentiation between Rapa Nui and Salas & Gómez Island (Chile), and between Meyer and Phillip islands (Australasia) that was not detected using mitochondrial DNA analyses. Within Hawaiʻi, we found a lack of significant genetic differentiation between Oʻahu and Kauaʻi, separated by 200 km. Our findings indicated that red-tailed tropicbird colonies are at genetic risk due to limited dispersal among colonies which may reduce the fitness of the species in the long-term. We suggest that red-tailed tropicbird colonies are vulnerable to future population declines because recovery through immigration from other islands may be limited by geographic distance. Conservation actions will help preserve genetic diversity and discrete populations for this native seabird at colonies throughout the Pacific.

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Acknowledgements

We are grateful to the Chilean Navy for transport to Salas & Gómez Island. We thank the indigenous community of Ma’u Henua and the National Forest Corporation-Rapa Nui (CONAF-Rapa Nui) for allowing access to the colony at Rano Raraku at the Rapa Nui National Park. We would like to acknowledge Nicolas Luna (PhD Candidate), Pedro Lazo and Graciela Campbell (CONAF-Rapa Nui rangers) for their help during fieldwork, and Dr. Miriam Lerma and Dr. Juan Serratosa for collecting some of the samples from Salas & Gómez used in this study. Karen Baird (Department of Conservation, manager Kermadec Islands Program at the time of sampling), Mark Hauber and Luis Ortiz-Catedral (Department of Conservation, Raoul team) helped with sample collection at North Meyer Islet, Kermadec, New Zealand. We also thanks team leader Margie Grant for field assistance and accommodation. Jesse Beck, Ryan Carle, Melinda Conners, Jonathan Felis, Cassidy Grattan, Seth Judge, Emma Kelsey, Caitlin Kroeger, and Olivia Townsend helped collect samples in Hawaiʻi. The Agricultural and Livestock Service (SAG), Chile authorized the bird’s manipulation protocol at Rapa Nui and Salas & Gómez Island. Thomas Kaʻiakapu, Jason Omick, Brooke McFarland, Heather Abbey, and Kim Uyehara kindly facilitated access and permitting in Hawaiʻi. The use of trade, product, or firm names in this publication is for descriptive purposes only and does not imply endorsement by the US Government. We thank Felipe Torres for the map confection shown in Fig. 1 and some image editing. Paula Demarco made the drawing of the red-tailed tropicbird shown on the map.

Funding

Funding for this project was provided by a postdoctoral research grant awarded to A I Varela (ANID-FONDECYT N°3160324), by the Millenium Nucleus for Ecology and Sustainable Management of Oceanic Islands (ESMOI), a Scientific Initiative supported by the Ministry of Economy, Development and Tourism (Chile), and by the ANID/FONDAP/15200002. Work in Hawaiʻi was supported in part by the Bureau of Ocean Energy Management (Interagency Agreement M13PG00022 with the U.S. Geological Survey, Western Ecological Research Center) and the USGS Ecosystems Mission Area.

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Authors and Affiliations

  1. Departamento de Oceanografía, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Concepción, Chile

    Andrea I Varela

  2. Center for Ecology and Sustainable Management of Oceanic Islands (ESMOI), Departamento de Biología Marina, Facultad de Ciencias del Mar, Universidad Católica del Norte, Coquimbo, Chile

    Andrea I Varela & Guillermo Luna-Jorquera

  3. Laboratorio de Fisiología y Genética Marina (FIGEMA), Departamento de Acuicultura, Facultad de Ciencias del Mar, Universidad Católica del Norte, Coquimbo, Chile

    Katherina Brokordt

  4. Centro de Estudios Avanzados en Zonas Áridas (CEAZA), Universidad Católica del Norte, Coquimbo, Chile

    Katherina Brokordt & Guillermo Luna-Jorquera

  5. Facultad de Ciencias Biológicas, Departamento de Ecología, Instituto para el Desarrollo Sustentable, Pontificia Universidad Católica de Chile, Millennium Institute Center for Genome Regulation (CRG), Millennium Institute of Biodiversity of Antarctic and Subantarctic Ecosystems (BASE), Santiago, Chile

    Juliana A Vianna

  6. Facultad de Medicina y Ciencia, Universidad San Sebastián, Valdivia, Chile

    María José Frugone

  7. Kurt-Ohlsen-Weg 1, D 24601, Ruhwinkel, Germany

    Stefanie MH Ismar-Rebitz

  8. School of Biological Sciences, University of Auckland, Auckland, New Zealand

    Stefanie MH Ismar-Rebitz

  9. Northern New Zealand Seabird Charitable Trust, Aotearoa New Zealand, 400 Leigh Road, RD5, Warkworth, Auckland, 0985, New Zealand

    Chris P Gaskin

  10. Department of Climate Change, Energy, the Environment and Water, Parramatta, New South Wales, Australia

    Nicholas Carlile & Terence O’Dwyer

  11. Western Ecological Research Center, US Geological Survey, Santa Cruz Field Station, Santa Cruz, California, USA

    Josh Adams

  12. Pacific Rim Conservation, Honolulu, Hawaiʻi, USA

    Eric A VanderWerf

Authors
  1. Andrea I Varela
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  2. Katherina Brokordt
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  3. Juliana A Vianna
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  4. María José Frugone
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  5. Stefanie MH Ismar-Rebitz
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  6. Chris P Gaskin
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  7. Nicholas Carlile
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  8. Terence O’Dwyer
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  9. Josh Adams
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  10. Eric A VanderWerf
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  11. Guillermo Luna-Jorquera
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Contributions

AIV and GLJ conceived the study. AIV collected samples in Chile, SIR, CPG, NC, TO, JA and EAV provided samples from New Zealand, Australia y Hawaiʻi. AIV, KB, and JAV conceptualized the manuscript. MJF analyzed the raw data, defined the dataset for analyses, and performed some of the analyses. AIV analyzed data and wrote the first draft of the manuscript. All authors contributed to previous versions of the manuscript and approved the final version for submission.

Corresponding author

Correspondence to Andrea I Varela.

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Ethical approval

Handling and sampling in Chile were approved by the Ethic-Scientific committee of Universidad Católica del Norte, sede Coquimbo, Chile. Field work, capture and sampling on Phillip Island, Australia, was carried out under Environmental Protection and Biodiversity Conservation Regulations 2000 scientific permit NI2018/09, Office of Environment and Energy Animal Ethics approval 021028-02. Field work, bird capture, banding and sampling in Hawaiʻi were authorized under U.S. Geological Survey Federal Bird Banding and Auxiliary Marking Authority Master Bander Permit #23843, U.S. Fish & Wildlife Service, Kilauea Point National Wildlife Refuge Research and Monitoring Special Use Permit #1253016005, Hawaiʻi Department of Land and Natural Resources, Division of Forestry and Wildlife, Protected Wildlife Permits #WL12-4 and #WL17-10, and Hawaiʻi Department of Land and Natural Resources, Division of Forestry and Wildlife, Lehua Seabird Sanctuary Special Use Permit Number KWSP-2016-14.

Competing interests

The authors declare no competing interests.

Additional information

Communicated by Xiaoli Shen.

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Varela, A.I., Brokordt, K., Vianna, J.A. et al. Are threatened seabird colonies of the pacific ocean genetically vulnerable? The case of the red-tailed tropicbird, Phaethon rubricauda, as a model species. Biodivers Conserv 33, 1165–1184 (2024). https://doi.org/10.1007/s10531-024-02791-3

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