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First study of the bat fossil record of the mid-Atlantic volcanic islands

Published online by Cambridge University Press:  03 December 2021

Javier GONZÁLEZ-DIONIS*
Affiliation:
Área de Paleontología, Facultad de Ciencias, Universidad de La Laguna, Av. Astrofísico Francisco Sánchez s/n, Apartado 456, San Cristobal de La Laguna, Tenerife, Spain. Universidad Nacional de Río Negro, Instituto de Investigación Paleobiología y Geología, Av. General Roca 1242, (8332) Roca, Río Negro, Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigación Paleobiología y Geología, Av. General Roca 1242, (8332) Roca, Río Negro, Argentina.
Carolina CASTILLO RUIZ
Affiliation:
Área de Paleontología, Facultad de Ciencias, Universidad de La Laguna, Av. Astrofísico Francisco Sánchez s/n, Apartado 456, San Cristobal de La Laguna, Tenerife, Spain.
Penélope CRUZADO-CABALLERO
Affiliation:
Área de Paleontología, Facultad de Ciencias, Universidad de La Laguna, Av. Astrofísico Francisco Sánchez s/n, Apartado 456, San Cristobal de La Laguna, Tenerife, Spain. Universidad Nacional de Río Negro, Instituto de Investigación Paleobiología y Geología, Av. General Roca 1242, (8332) Roca, Río Negro, Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigación Paleobiología y Geología, Av. General Roca 1242, (8332) Roca, Río Negro, Argentina.
Elena CADAVID-MELERO
Affiliation:
Área de Paleontología, Facultad de Ciencias, Universidad de La Laguna, Av. Astrofísico Francisco Sánchez s/n, Apartado 456, San Cristobal de La Laguna, Tenerife, Spain.
Vicente D. CRESPO
Affiliation:
División Paleontología Vertebrados, Consejo Nacional de Investigaciones Científicas y Técnicas, Museo de La Plata, Paseo del Bosque s/n, B1900FWA, La Plata, Argentina. Museo Paleontológico de Alpuente, Av. San Blas 17, Alpuente, 46178 Valencia, Spain. Museu Valencià d'Història Natural, L'Hort de Feliu, PO Box 8460, Alginet, 46230 Valencia, Spain.
*
*Corresponding author. Email: jagondi1@gmail.com

Abstract

Bats are one of the most abundant and important mammals in ecosystems. However, their fossil record is scarce and fragile, making them difficult to find. Accordingly, there is no record of this group in the volcanic islands of the mid-Atlantic Ocean apart from the Canary Islands. This paper studies the first bat fossil record of the Canary Islands (Spain). The material studied is found within two Quaternary lava tubes, Cueva de los Verdes on Lanzarote and Cueva Roja on the island of El Hierro. The dental and humeral morphology and biometry are analysed and compared with current specimens. Among our results we highlight the first fossil data of two species endemic to the islands of the mid-Atlantic Ocean, Plecotus teneriffae and Pipistrellus maderensis, the former from the Canary Islands and the latter from the Azores, Madeira and the Canary Islands. We also confirm the presence of Pipistrellus kuhlii in the fossil record of the island of Lanzarote. No differences are observed between the dental morphology of the current and the fossil populations of P. maderensis and Pl. teneriffae. In the case of P. kuhlii, the populations of the Canary Islands and the Iberian Peninsula show differences in the paraconule with respect to the populations from central Europe. Palaeoecological studies of these taxa suggest that these islands presented a similar habitat when the sites were formed to the present-day habitat.

Type
Articles
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of The Royal Society of Edinburgh

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References

7. References

Ahmim, M. 2017. Current status, distribution and conservation status of Algerian bats (Mammalia: Chiroptera). Journal of Threatened Taxa 9, 9723-9733.CrossRefGoogle Scholar
Alcaldé, J. & Juste, J. 2016a. Pipistrellus maderensis. The IUCN Red List of Threatened Species 2016: e.T17315A1380378. https://dx.doi.org/10.2305/IUCN.UK.2016-2.RLTS.T17315A1380378.en (accessed 9 November 2020).CrossRefGoogle Scholar
Alcaldé, J & Juste, J. 2016b. Plecotus teneriffae. The IUCN Red List of Threatened Species 2016: e.T17602A1424721. https://dx.doi.org/10.2305/IUCN.UK.2016-2.RLTS.T17602A1424721.en (accessed 9 November 2020).CrossRefGoogle Scholar
Asociación Española para la Conservación y el Estudio de los Murciélagos. 2019. Los murciélagos en España, Portugal y Gibraltar. http://secemu.org/murcielagos/los-murcielagos-espana/ (accessed 3 August 2019).Google Scholar
Banco de Datos de Biodiversidad de Canarias. 2021. https://www.biodiversidadcanarias.es/biota/ (accessed 21 October 2020).Google Scholar
Benda, P., Kiefer, A., Hanák, V. & Veith, M. 2004. Systematic status of African populations of long-eared bats, genus Plecotus (Mammalia: Chiroptera). Folia Zoologica 53(Monogr. 1), 1–47.Google Scholar
Benda, P. & Piraccini, R. 2016. Tadarida teniotis. The IUCN Red List of Threatened Species 2016: e.T21311A22114995. https://dx.doi.org/10.2305/IUCN.UK.2016-2.RLTS.T21311A22114995.en (accessed 9 November 2020).CrossRefGoogle Scholar
Benzal, J. & Fajardo, S. 1997. Murciélagos de España. Galemys 9, 414.Google Scholar
Benzal, J. & Fajardo, S. 1999. Plecotus teneriffae. In Mitchell-Jones, A. J., Amori, G., Bogdanowicz, W., Kryštufek, B., Reijnders, P. J. H., Spitzenberger, F., Stubbe, M., Thissen, J. B. M., Vohralík, V. & Zima, J. (eds.) The atlas of European mammals, 152153. London: Academic Press.Google Scholar
Borloti, I., Dinis, H. & Vasconcelos, R. 2020. Bats out of Africa: disentangling the systematic position and biogeography of bats in Cabo Verde. Genes 11, 123.CrossRefGoogle ScholarPubMed
Bravo, T. 1964. El volcán y el malpaís de la Corona: La “Cueva de los Verdes” y los “Jameos”. Arrecife, Spain: Cabildo Insular de Lanzarote.Google Scholar
Brown, E. E., Cashmore, D. D., Simmons, N. B. & Butler, R. J. 2019. Quantifying the completeness of the bat fossil record. Palaeontology 62, 757–76.CrossRefGoogle Scholar
Carracedo, J., Singer, B., Jicha, B., Guillou, H., Rodriguez, E., Meco, J., Pérez-Torrado, F. J., Gimeno, D., Socorro, S. & Lainez, A. 2003. La erupcion y el tubo volcanico del Volcan Corona. Estudios Geológicos 59, 277302.CrossRefGoogle Scholar
Castillo, C., López, M., Martín, M. & Rando, J. C. 1996. La paleontología de vertebrados en Canarias. [The vertebrate paleontology in Canary Islands]. Revista Española de Paleontología Nº Extraordinario, 237247.Google Scholar
Cooper-Bohannon, R., Mickleburgh, S., Hutson, A. M., Bergmans, W., Fahr, J. & Racey, P. A. 2020. Eidolon helvum. The IUCN Red List of Threatened Species 2020: e.T7084A22028026. https://dx.doi.org/10.2305/IUCN.UK.2020-2.RLTS.T7084A22028026.en (accessed 9 November 2020).CrossRefGoogle Scholar
Coroiu, I., Juste, J. & Paunović, M. 2016. Myotis myotis. The IUCN Red List of Threatened Species 2016: e.T14133A22051759. https://dx.doi.org/10.2305/IUCN.UK.2016-2.RLTS.T14133A22051759.en. (accessed on 20 November 2021).Google Scholar
Crespo, V. D., Sevilla, P., Mansino, S., Montoya, P. & Ruiz-Sánchez, F. 2018. Bats from the classical site of Venta del Moro (Late Miocene, Eastern Spain). Historical Biology 30, 317–26.CrossRefGoogle Scholar
Crespo, V. D., Sevilla, P., Montoya, P. & Ruiz-Sánchez, F. 2020. A relict tropical forest bat assemblage from the early Miocene of the Ribesalbes-Alcora Basin (Castelló, Spain). Earth and Environmental Science Transactions of the Royal Society of Edinburgh 111, 247258.CrossRefGoogle Scholar
Del Arco, M. J. & Rodríguez, O. 2018. Vegetation of the canary islands. Cham: Springer.CrossRefGoogle Scholar
Diego Cuscoy, L. 1972. Excavaciones arqueológicas en Tegueste. La necrópolis de ‘La Enladrillada’ (Tegueste, Tenerife). Noticiario Arqueológico Hispánico 1, 271313.Google Scholar
Dupuis, I. 1986. Les Chiropteres du Quaternaire en France. Mémoire de Maîtrise de l'Université de Paris I. Paris.Google Scholar
Fajardo, S. & Benzal, J. 2002. Data on the distribution of bats in the Canary Islands (Mammalia: Chiroptera). VIERAEA 30, 213–30.Google Scholar
Frick, W. F., Kingston, T. & Flanders, J. 2019. A review of the major threats and challenges to global bat conservation. Annals of the New York Academy of Sciences 1469, 525.CrossRefGoogle ScholarPubMed
Fukui, D., Tu, V. T., Thanh, H. T., Arai, S., Harada, M., Csorba, G. & Son, N. T. 2020. First record of the genus Plecotus from Southeast Asia with notes on the taxonomy, karyology and echolocation call of P. homochrous from Vietnam. Acta Chiropterologica 22, 5774.CrossRefGoogle Scholar
Fuster, J. M., Hernán, F., Cendrero, A., Coello, J., Cantagrel, J. M., Ancochea, E., Ibarrola, E. 1993. Geocronologia de la Isla de El Hierro (Islas Canarias). Boletin – Real Sociedad Española de Historia Natural: Seccion Geologica 88, 8597.Google Scholar
Galán, J., Núñez-Lahuerta, C., López-García, J. M. & Cuenca-Bescós, G. 2019a. Did humans disturb bats? Exploring the hominin-chiropter interactions in the Sierra de Atapuerca sites (early to Middle Pleistocene, Spain). Quaternary Science Reviews 226, 106018.CrossRefGoogle Scholar
Galán, J., Núñez-Lahuerta, C., Sauqué, V., Cuenca-Bescós, G. & López-García, J. M. 2019b. Cranial biometrics of the Iberian Myotis myotis/Myotis blythii complex: new data for studying the fossil record. Journal of Mammalian Evolution 26, 333–44.CrossRefGoogle Scholar
Gazaryan, S., Bücs, S. & Çoraman, E. 2020. Miniopterus schreibersii. The IUCN Red List of Threatened Species 2020: e.T81633057A151216401. https://dx.doi.org/10.2305/IUCN.UK.2020-2.RLTS.T81633057A195856522.en (accessed 9 November 2020).CrossRefGoogle Scholar
Gazaryan, S. & Godlevska, L. 2020. Plecotus austriacus. The IUCN Red List of Threatened Species 2020: e.T85533333A85533603. https://dx.doi.org/10.2305/IUCN.UK.2021-1.RLTS.T85533333A195862345.en (accessed 9 November 2020).CrossRefGoogle Scholar
Godlevska, L., Bücs, S., Kruskop, S.V., Gazaryan, S., Benda, P. & Paunović, M. 2020. Pipistrellus pipistrellus. The IUCN Red List of Threatened Species 2020: e.T85333513A22132116.Google Scholar
Govantes, R. & García, F. 2013. PROPUESTA DE TUBOS VOLCÁNICOS COMO NUEVOS ESPACIOS NATURALES PROTEGIDOS EN LA ISLA DE LA PALMA (CANARIAS). Vulcania. Revista de Espeleología del Archipiélago Canario 10, 512.Google Scholar
Gunnell, G. F. & Simmons, N. B. 2005. Fossil evidence and the origin of bats. Journal of Mammalian Evolution 12, 209–46.CrossRefGoogle Scholar
Hernández, J., Medina, A. & Izquierdo, I. 1992. Volcanic caves in El Hierro Island, Canary Islands, Spain. In 6th International Symposium on Vulcanospeleology. Hilo, Hawaii (August 1991), 185–96.Google Scholar
Hukov, V., Timofieieva, O., Prylutska, A., Rodenko, O., Moiseienko, M., Bohodist, V., Domanska, A. & Vlaschenko, A. 2020. Wintering of an urban bat (Pipistrellus kuhlii lepidus) in recently occupied areas. European Journal of Ecology 6, 102–20.CrossRefGoogle Scholar
Hutterer, R., Ivanova, T., Meyer-Cord, C. & Rodrigues, L. 2005. Bat migrations in Europe. Naturschutz und Biologische Vielfalt 28, 162.Google Scholar
Jablonski, D. & Shubin, N. H. 2015. The future of the fossil record: paleontology in the 21st century. Proceedings of the National Academy of Sciences 112, 4852–58.CrossRefGoogle ScholarPubMed
Jepsen, G. L. 1966. Early Eocene bat from Wyoming. Science 154, 1333–39.CrossRefGoogle ScholarPubMed
Jesus, J., Teixeira, S., Freitas, T., Teixeira, D. & Brehm, A. 2013. Genetic identity of Pipistrellus maderensis from the Madeira archipelago: a first assessment, and implications for conservation. Hystrix, the Italian Journal of Mammalogy 24, 177180.Google Scholar
Jiménez, S. & Hazevoet, C. J. 2010. First record of Straw-coloured fruit bat Eidolon helvum (Kerr, 1792) for the Cape Verde Islands. Zoologia Caboverdiana 1, 116-118.Google Scholar
Juste, J. & Paunović, M. 2016a. Pipistrellus kuhlii. The IUCN Red List of Threatened Species 2016: e.T17314A22132946. https://dx.doi.org/10.2305/IUCN.UK.2016-2.RLTS.T17314A22132946.en (accessed 9 November 2020).CrossRefGoogle Scholar
Juste, J. & Paunović, M. 2016b. Hypsugo savii. The IUCN Red List of Threatened Species 2016: e.T44856A22072380. https://dx.doi.org/10.2305/IUCN.UK.2016-3.RLTS.T44856A22072380.en (accessed 9 November 2020).CrossRefGoogle Scholar
Juste, J. & Paunović, M. 2016c. Nyctalus leisleri. The IUCN Red List of Threatened Species 2016: e.T14919A22016159. https://dx.doi.org/10.2305/IUCN.UK.2016-2.RLTS.T14919A22016159.en (accessed 9 November 2020).CrossRefGoogle Scholar
Juste, J., Ibáñez, C., Muñoz, J., Trujillo, D., Benda, P., Karataş, A. & Ruedi, M. 2004. Mitochondrial phylogeography of the long-eared bats (Plecotus) in the Mediterranean Palaearctic and Atlantic Islands. Plecotus 31, 11141126.Google ScholarPubMed
Lindenau, C. 2005. Middle Pleistocene bats (Mammalia: Chiroptera) from the Yarimburgaz Cave in Turkish Thrace (Turkey). Eiszeitalter und Gegenwart. Quaternary Science Journal 55, 122–48.Google Scholar
Lomoschitz, A., Sánchez Marco, A., Huertas, M. J., Betancort, J. F., Isern, A., Sanz, E. & Meco, J. 2016. A reappraisal of the stratigraphy and chronology of Early Pliocene palaeontological sites from Lanzarote Island containing fossil terrestrial animals. Journal of African Earth Sciences 123, 338–49.CrossRefGoogle Scholar
Lopes, M. & Medeiros, F. 2011. Revisão sobre os morcegos do arquipelago dos Açores contribuição para a sua conservação. XV Expedição Científica do Departamento de Biologia - São Jorge 40, 98.Google Scholar
Marchese, C. 2015. Biodiversity hotspots: a shortcut for a more complicated concept. Global Ecology and Conservation 3, 297309.CrossRefGoogle Scholar
Masseti, M. 2010. Mammals of the Macaronesian islands (the Azores, Madeira, the Canary and Cape Verde islands): redefinition of the ecological equilibrium. Mammalia 74, 334.CrossRefGoogle Scholar
Menu, H. 1987. Morphotypes dent aires actuels et fossiles des Chiropteres Vespertilionines 2eme partie: implications systematiques et phylogeniques. Palaeovertebrata 17, 77150.Google Scholar
Monadjem, A., Racey, P.A., Amr, Z.S.S., Fahr, J., Palmeirim, J., Benda, P., Bates, P., Aulagnier, S., Bergmans, W., Hutson, A.M. & Kock, D. 2017. Taphozous nudiventris. The IUCN Red List of Threatened Species 2017: e.T21462A22109884. https://dx.doi.org/10.2305/IUCN.UK.2017-2.RLTS.T21462A22109884.en (accessed 9 November 2020).CrossRefGoogle Scholar
Moreno, J.M. 1992. Fauna de las Islas Canarias. Tenerife: Ediciones Turquesa, pp. 23.Google Scholar
Palmeirim, J. M. 1979. First Record of Myotis myotis on the Azores Islands: (Chiroptera: Vespertilionidae). Museu Bocage, Faculdade de Ciências.Google Scholar
Palmeirim, J. M. 1991. A morphometric assessment of the systematic position of the Nyctalus from Azores and Madeira (Mammalia: Chiroptera).CrossRefGoogle Scholar
Palomo, L. J., Gisbert, J. & Blanco, J. C. 2007. Atlas y Libro Rojo de los Mamíferos Terrestres de España. Dirección General para la Biodiversidad-SECEM-SECEMU, Madrid, 588 pp.Google Scholar
Pérez-Torrado, F. J., Carracedo, J. C., Rodríguez-Gonzalez, A., Soler, V., Troll, V. R. & Wiesmaier, S. 2012. La erupción submarina de La Restinga en la isla de El Hierro, Canarias: Octubre 2011–Marzo 2012 [The submarine eruption of La Restinga (El Hierro, Canary Islands): October 2011–March 2012]. Estudios Geológicos 68, 527.Google Scholar
Perez-Torrado, F. J., Rodriguez-Gonzalez, A., Carracedo, J. C., Fernandez-Turiel, J. L., Guillou, H., Hansen, A. & Rodríguez Badiola, E. 2011. Edades C-14 Del Rift ONO de El Hierro (Islas Canarias). Resúmenes XIII Reunión Nacional de Cuaternario. Andorra 2011.Google Scholar
Pestano, J., Brown, R. P., Suárez, N. M. & Fajardo, S. 2003. Phylogeography of pipistrelle-like bats within the Canary Islands, based on mtDNA sequences. Molecular Phylogenetics and Evolution 26, 5663.CrossRefGoogle ScholarPubMed
Piraccini, R. 2016a. Barbastella barbastellus. The IUCN Red List of Threatened Species 2016: e.T2553A22029285. https://dx.doi.org/10.2305/IUCN.UK.2016-2.RLTS.T2553A22029285.en (accessed 9 November 2020).CrossRefGoogle Scholar
Piraccini, R. 2016b. Nyctalus azoreum. The IUCN Red List of Threatened Species 2016: e.T14922A546843. https://dx.doi.org/10.2305/IUCN.UK.2016-2.RLTS.T14922A546843.en (accessed 9 November 2020).CrossRefGoogle Scholar
Riccucci, M. & Lanza, B. 2014. Bats and insect pest control: a review. Vespertilio 17, 161–69.Google Scholar
Rosina, V. V. & Sinitsa, M. V. 2014. Bats (Chiroptera, Mammalia) from the Turolian of the Ukraine: phylogenetic and biostratigraphic considerations. Neues Jahrbuch Für Geologie Und Paläontologie - Abhandlungen 272, 147166.CrossRefGoogle Scholar
Sachanowicz, K., Bogdanowicz, W. & Michalak, S. 1999. First record of Taphozous nudiventris Cretzschmar, 1830 (Chiroptera, Emballonuridae) in Turkey. Mammalia 63, 105-107.Google Scholar
Salles, L. O., Arroyo-Cabrales, J., do Monte Lima, A. C., Lanzelotti, W., Perini, F. A., Velazco, P. M. & Simmons, N. B. 2014. Quaternary bats from the Impossível-Ioiô Cave system (Chapada Diamantina, Brazil): humeral remains and the first fossil record of Noctilio leporinus (Chiroptera, Noctilionidae) from South America. American Museum Novitates 3798, 131.CrossRefGoogle Scholar
Sevilla, P. 1986. Identificación de los principales quirópteros ibéricos a partir de sus dientes aislados: valor sistemático de los caracteres morfológicos y métricos dentarios. Acta vertebrata 13, 111–30.Google Scholar
Sevilla, P. 1988. Estudio paleontológico de los quirópteros del cuaternario Español. Universidad Complutense de Madrid, Spain.Google Scholar
Sevilla, P. & López Martínez, N. 1986. Comparative systemic value between dental and external/skeletal features in western European Chiroptera. In VIIth International Symposium on Dental Morphology, Paris, 1986. Russell D. E., Santoro J.-P. & Sigogneau-Russell D., Eds Mém. Mus. natn. Hist. nat., Paris (série C) 53: 255–266.Google Scholar
Simmons, N. B. & Cirranello, A. L. 2019. Bat species of the world: a taxonomic and geographic database. www.batnames.org (accessed 4 August 2019).Google Scholar
Simmons, N. B., Seymour, K. L., Habersetzer, J. & Gunnell, G. F. 2008. Primitive Early Eocene bat from Wyoming and the evolution of flight and echolocation. Nature 451, 818–21.CrossRefGoogle ScholarPubMed
Spitzenberger, F., Strelkov, P. P., Winkler, H. & Haring, E. 2006. A preliminary revision of the genus Plecotus (Chiroptera, Vespertilionidae) based on genetic and morphological results. Zoologica Scripta 35, 187230.CrossRefGoogle Scholar
Steiner, C., Lausanne, C. & Hernandez, J. 1998. Mesozoic sequence of Fuerteventura (Canary Islands): witness of Early Jurassic sea-floor spreading in the central Atlantic. Geological Society of America Bulletin 110, 1304–17.2.3.CO;2>CrossRefGoogle Scholar
Torre, G., Fernández-Lugo, S., Guarino, R. & Fernández-Palacios, J. M. 2018. Network analysis by simulated annealing of taxa and islands of Macaronesia (North Atlantic Ocean). Ecography 42, 768–79.CrossRefGoogle Scholar
Troll, V. & Carracedo, J. 2016. The geology of the Canary Islands Elsevier.Google Scholar
Trujillo, D. 1991. Murciélagos de las Islas Canarias. Madrid: Icona.Google Scholar
Trujillo, D. 2011. Nuevas citas de murciélago rabudo Tadarida teniotis (Rafinesque, 1814) en Gran Canaria, islas Canarias (Chiroptera, Molossidae). Vieraea: Folia Scientarum Biologicarum Canariensium 39, 225228.Google Scholar
Trujillo, D. & González, C. 2011. Pipistrellus maderensis (Dobson, 1878) (Chiroptera: Vespertilionidae), una nueva adición a la fauna de las islas Azores (Océano Atlántico). VIERAEA 39, 215–18.Google Scholar
Trujillo, D., Ibáñez, C. & Juste, J. 2002. A new subspecies of Barbastella barbastellus (Mammalia: Chiroptera: Vespertilionidae) from the Canary islands. Revue suisse de Zoologie 109, 543–550.Google Scholar
Trujillo, D., Tosco, R. B. & García, D. (2012). Estatus y distribución del murciélago montañero Hypsugo savii (Bonaparte, 1837) en Gran Canaria, islas Canarias (Chiroptera: Vespertilionidae). Vieraea: Folia Scientarum Biologicarum Canariensium 40, 155158.Google Scholar
Vasconcelos, R. 2018. Bibliographic revision and new records of bats (Chiroptera) for Cabo Verde Archipelago. Zoologia Caboverdiana 7, 311.Google Scholar