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Untangling the origin of the newcomer Phorcus sauciatus (Mollusca: Gastropoda) in a remote Atlantic archipelago

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Abstract

The marine topshell Phorcus sauciatus is currently found along the temperate–subtropical shores of the Northeast Atlantic Ocean. Although present in the Iberian Peninsula, Madeira, and Canaries for centuries, P. sauciatus has only recently reached another oceanic volcanic archipelago in the region. In 2013, a small population was recorded for the first time in Santa Maria Island (Azores), widening its distribution around the entire island and to the neighbouring island of São Miguel in a short period of time. The success of such colonization of the remote archipelago by P. sauciatus still awaits an explanation. To better understand the populational dynamics of the species in the NE Atlantic Ocean, we used a molecular approach to evaluate the genetic structure of P. sauciatus aiming at the determination of a potential origin for the first individuals that reached the Azores. On the foundations of detailed oceanographic, palaeontological, and ecological data, we discuss the impact of climate change as a trigger for colonization of remote oceanic islands and suggest a mechanism that might explain the long-distance dispersal of the non-planktotrophic gastropod P. sauciatus across important biogeographical barriers in the NE Atlantic.

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Data availability

The datasets generated during the current study are available in the GenBank Nucleotide Database at https://www.ncbi.nlm.nih.gov/genbank/ and can be accessed with accession numbers MT474920-38 and MW094272-304. Other data analysed in the current study are also available at the same repository, under the accession numbers KC990609-16; KC990625-31; JN241978-94; KJ818223; JN686319-20; JN686325-7; JN686299-313; KF369166; KU496657-73; KU566798-9.

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Acknowledgments

This work was supported by Fundação para a Ciência e Tecnologia, IP (PhD grant SFRH/BD/135918/2018 to LB; research contract IF/00465/2015 to SPA; Post-doctoral grant SFRH/BPD/117810/2016 to ACR) and FRCT/Açores 2020 by Fundo Regional para a Ciência e Tecnologia (FRCT) (grant M3.1.a/F/100/2015 to CSM). This work benefits from FEDER funds through the Operational Programme for Competitiveness Factors – COMPETE and national funds through Fundação para a Ciência e Tecnologia, IP (projects UID/BIA/50027/2013, POCI-01-0145-FEDER-006821); by regional funds through Direção Regional para a Ciência e Tecnologia (DRCT-M1.1.a/005/Funcionamento-C-/2016). This work was also supported by FEDER funds (85 %) and by funds of the Regional Government of the Azores (15%) through Programa Operacional Açores 2020, in the scope of the projects “VRPROTO”: Virtual Reality PROTOtype: the geological history of “Pedra-que-pica”: ACORES-01-0145-FEDER-000078, and “AZORESBIOPORTAL – PORBIOTA”: ACORES-01-0145-FEDER-000072. AV acknowledges FCT funding from grants IF/01500/2014 and UIDB/04326/2020. We thank João Gonçalves (OKEANOS/Universidade dos Açores), João Faria (Univ. Azores), João Brum (Univ. Azores) and Isadora Moniz (Univ. Lisbon) for information used in this study. We acknowledge the governmental entities for the sampling licenses: 01/ICFN/2019-FAU MAD (Regional Government of Madeira) and CCPI 24/2019/DRCT (Regional Government of the Azores). We thank the reviewers, whose comments and suggestions greatly improved the manuscript.

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Authors and Affiliations

  1. CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Pólo dos Açores, 9501-801, Ponta Delgada, Portugal

    Lara Baptista, Carlos S. Melo, Ana C. Rebelo, Patrícia Madeira, Ricardo Cordeiro, Andrea Z. Botelho & Sérgio P. Ávila

  2. MPB-Marine Palaeontology and Biogeography Lab, Universidade dos Açores, Rua da Mãe de Deus, 9501-801, Ponta Delgada, Portugal

    Lara Baptista, Carlos S. Melo, Ana C. Rebelo, Patrícia Madeira, Ricardo Cordeiro, Andrea Z. Botelho, Joana Pombo & Sérgio P. Ávila

  3. Faculdade de Ciências da Universidade do Porto, Rua do Campo Alegre, 1021/1055, 4169-007, Porto, Portugal

    Lara Baptista, António M. Santos & Sérgio P. Ávila

  4. CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Universidade do Porto, Campus de Vairão, Rua Padre Armando Quintas, no. 7, 4485-661, Vairão, Portugal

    António M. Santos

  5. Departamento de Geologia, Faculdade de Ciências, Universidade de Lisboa, 1749-016, Lisboa, Lisbon, Portugal

    Carlos S. Melo

  6. Instituto Dom Luiz, Faculdade de Ciências, Universidade de Lisboa, 1749-016, Lisboa, Lisbon, Portugal

    Carlos S. Melo & Ana Hipólito

  7. Divisão de Geologia Marinha, Instituto Hidrográfico, Rua das Trinas, 49, 1249-093, Lisboa, Portugal

    Ana C. Rebelo

  8. SMNS - Staatliches Museum Für Naturkunde Stuttgart, Rosenstein 1, 70191, Stuttgart, Germany

    Ana C. Rebelo

  9. Departamento de Biologia, Faculdade de Ciências e Tecnologia, Universidade dos Açores, 9501-801, Ponta Delgada, Portugal

    Patrícia Madeira, Ricardo Cordeiro & Sérgio P. Ávila

  10. IVAR – Instituto de Investigação em Vulcanologia e Avaliação de Riscos, Faculdade de Ciências e Tecnologia, Universidade Dos Açores, 9501-801, Ponta Delgada, Açores, Portugal

    Ana Hipólito

  11. Centro de Interpretação Ambiental Dalberto Pombo, Rua Teófilo Braga no. 14, 9580-535, Vila do Porto, Portugal

    Joana Pombo

  12. IPMA – Instituto Português do Mar e da Atmosfera, Divisão de Geologia e Georecursos Marinhos, Av. Doutor Alfredo Magalhães Ramalho, 6, 1495-165, Algés, Portugal

    Antje H. L. Voelker

  13. CCMAR – Centre of Marine Sciences, University of Algarve, 8005-139, Faro, Portugal

    Antje H. L. Voelker

Authors
  1. Lara Baptista
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  2. António M. Santos
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  3. Carlos S. Melo
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  4. Ana C. Rebelo
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  5. Patrícia Madeira
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  6. Ricardo Cordeiro
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  7. Andrea Z. Botelho
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  8. Ana Hipólito
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  9. Joana Pombo
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  10. Antje H. L. Voelker
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  11. Sérgio P. Ávila
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Contributions

Initial framework by LB, AMS, and SPA. The writing was led by LB, SPA, and AMS, and all co-authors equally contributed to its final design. Fieldwork was performed at Santa Maria by LB, SPA, ACR, AH, CSM, AZB, JP, PM, and ACR; at São Miguel and Madeira by LB. The genetic work was conducted by LB and AMS. The oceanographic bibliography review was made by AHLV. Biogeographic-related bibliography review was made by LB and SPA. Figures were made by CSM, AHLV, and LB. All authors approved the final version.

Corresponding author

Correspondence to Lara Baptista.

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Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

New COI sequences of P. sauciatus were obtained from specimens deposited in the Marine Molluscs Reference Collection of the Department of Biology of the University of the Azores (DBUA) or from fresh samples collected in several locations in the Azores Archipelago. Sampling permits were issued by the respective authorities in the Azores (Direção Regional da Ciência e Tecnologia, Governo Regional dos Açores; CCIP 24/2019/DRCT) and Madeira (Secretaria Regional do Ambiente e Recursos Naturais, Governo Regional da Madeira; permit 01/IFCN/2019-FAU MAD). Additional COI sequences were retrieved from the GenBank database. All applicable national and/or institutional guidelines for the use of collection material were followed. Only invertebrates were used in this study.

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Baptista, L., Santos, A.M., Melo, C.S. et al. Untangling the origin of the newcomer Phorcus sauciatus (Mollusca: Gastropoda) in a remote Atlantic archipelago. Mar Biol 168, 9 (2021). https://doi.org/10.1007/s00227-020-03808-5

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