Abstract
This study aimed to (i) evaluate species richness and endemicity for the stygobiont oligochaete taxa (Annelida, Clitellata) in the Cantabrian region of northern Spain; and (ii) identify the environmental factors that determine the stygobiont assemblages at the regional scale. We recorded and examined more than 7,000 specimens of groundwater oligochaetes from 58 sampling sites. Of 62 identified species, 15 were classified as stygobionts, raising the known stygobiont oligochaete richness in the Cantabrian region to 21 species. As a result, the region is the second richest area for stygobiont oligochaete fauna in Europe after Slovenia with 28 species. Stygobiont oligochaetes exhibited a high degree of endemicity: 9 stygobionts were endemic to their type localities and 8 were restricted to geographic areas of less than 240 km in length, which underlines the narrow geographic ranges for subterranean fauna. Differences among the karsts were observed but the measured environmental factors did not explain the structure of the stygobiont assemblages in the Cantabrian region. Electrical conductivity, latitude and longitude influenced stygobiont species distributions but correlation values were low. Other ecological and historical factors should be evaluated in future; in particular, marine transgressions–regressions may have played a major role as evidenced by the large number of stygobionts of marine origin (8 species) found in both coastal and inland karsts.
Similar content being viewed by others
References
Achurra, A. & P. Rodriguez, 2008. Biodiversity of groundwater oligochaetes from a karst unit in northern Iberian Peninsula: ranking subterranean sites for conservation management. Hydrobiologia 605: 159–171.
Achurra, A., M. A. Elejalde & P. Rodriguez, 2011. Phylogenetic analysis of oligochaete Tubificinae (Annelida: Clitellata) based on mitochondrial sequence data. Invertebrate Systematics 25: 208–218.
Achurra, A., M. Creuze Des Chatelliers & P. Rodriguez, 2012. Troglodrilus jugeti n. sp. (Annelida, Clitellata, Tubificinae), a new stygobiont oligochaete species from south-western Europe. Zootaxa 3229: 35–46.
Bellés, X., 1987. Fauna cavernícola i intersticial de la Península ibérica i les illes Balears. Consell superior d’investigacions científiques-Editorial Moll, Mallorca.
Boutin, C. & N. Coineau, 1990. Regression model evolution, two-step model evolution and the origin of continental stygobiontic interstitial microfauna. Revue de Micropaléontologie 33: 303–322.
Camacho, A. I., A. G. Valdecasas, J. Rodriguez, S. Cuezva, J. Lario & S. Sanchez-Moral, 2006. Habitat constraints in epikarstic waters of an Iberian Peninsula cave system. Annales de Limnologie—International Journal of Limnology 42: 127–140.
Castellarini, F., F. Malard, M. J. Dole-Olivier & J. Gibert, 2007. Modelling the distribution of stygobionts in the Jura Mountains (eastern France) Implications for the protection of ground waters. Diversity and Distributions 13: 213–224.
Clarke, K. R. & R. N. Gorley, 2006. PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth.
Colwell, R. K., 2013. EstimateS: Statistical Estimation of Species Richness and Shared Species from Samples, Version 9 [available on internet at http://www.purloclcorg/estimates]. Accessed 01 March 2014.
Colwell, R. K., C. X. Mao & J. Chang, 2004. Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85: 2717–2727.
Colwell, R. K., A. Chao, N. J. Gotelli, S. Y. Lin, C. X. Mao, R. L. Chazdon & J. T. Longino, 2012. Models and estimators linking individual-based and sample-based rarefaction, extrapolation, and comparison of assemblages. Journal of Plant Ecology 5: 3–21.
Corrin, J. S. & P. Smith, 1981. Matienzo underground. Transactions of the British Cave Research Association 8: 87–110.
Culver, D. C. & T. Pipan, 2009. The Biology of Caves and Other Subterranean Habitats. Oxford University Press, New York.
Culver, D. C. & B. Sket, 2000. Hotspots of subterranean biodiversity in caves and wells. Journal of Cave and Karst Studies 62: 11–17.
Culver, D. C., L. Deharveng, A. Bedos, J. J. Lewis, M. Madden, J. R. Reddell, B. Sket, P. Trontelj & D. White, 2006a. The mid-latitude biodiversity ridge in terrestrial cave fauna. Ecography 29: 120–128.
Culver, D. C., T. Pipan & K. Schneider, 2006b. Hypothelminorheic – a unique freshwater habitat. Subterranean Biology 4: 1–8.
Culver, D. C., P. Trontelj, M. Zagmajster & T. Pipan, 2013. Paving the Way for Standardized and Comparable Subterranean Biodiversity Studies. Subterranean Biology 10: 43–50.
Danielopol, D. L., R. Rouch & A. Baltanas, 2002. Taxonomic diversity of groundwater harpacticoida (Copepoda, Crustacea) in Southern France. Vie Milieu 52: 1–15.
Deharveng, L., F. Stoch, J. Gibert, A. Bedos, D. Galassi, M. Zagmajster, A. Brancelj, A. Camacho, F. Fiers, P. Martin, N. Giani, G. magniez & P. Marmonier, 2009. Groundwater biodiversity in Europe. Freshwater Biology 54: 709–726.
Delay, B., 1973. Deux nouveaux Oligochètes Haplotaxidae troglobies d’Espagne: Haplotaxis navarrensis n sp. et Haplotaxis cantabronensis n sp. Anales de Spéléologie 28: 405–411.
Des Châtelliers, M. C., J. Juget, M. Lafont & P. Martin, 2009. Subterranean aquatic Oligochaeta. Freshwater Biology 54: 678–690.
Díaz, J., J. Gallart, D. Pedreira, J. A. Pulgar, M. Ruiz, C. López & J. M. González-Cortina, 2003. Teleseismic imaging of alpine crustal underthrusting beneath N-Iberia. Geophysical Research Letters 30: 1554.
Dole-Olivier, M. J., F. Castellarini, N. Coineau, D. M. P. Galassi, P. Martin, N. Mori, A. Valdecasas & J. Gibert, 2009. Towards an optimal sampling strategy to assess groundwater biodiversity: comparison across six European regions. Freshwater Biology 54: 777–796.
Erséus, C., M. J. Wetzel & L. Gustavsson, 2008. ICZN rules – a farewell to Tubificidae (Annelida, Clitellata). Zootaxa 1744: 66–68.
Farara, D. G. & C. Erséus, 1991. Phallodrilus aquaedulcis Hrabĕ, 1960, a meiobenthic freshwater oligochaete (Tubificidae) previously known only from Europe, recorded from the Niagra River, North America. Canadian Journal of Zoology 69: 291–294.
Ferreira, D., F. Malard, M. J. Dole-Olivier & J. Gibert, 2007. Obligate groundwater fauna of France: diversity patterns and conservation implications. Biodiversity and Conservation 16: 567–596.
Galassi, D. M., F. Stoch, B. Fiasca, T. Di Lorenzo & E. Gattone, 2009. Groundwater biodiversity patterns in the Lessinian Massif of Northern Italy. Freshwater Biology 54: 830–847.
Giani, N. & P. Rodriguez, 1988. Description de quelques espèces nouvelles de Tubificidae (Oligochaeta) de grottes et de sources karstiques de la péninsule ibérique. Stygologia 4: 121–137.
Giani, N. & P. Rodriguez, 1994. New species of the genus Trichodrilus (Oligochaeta, Lumbriculidae). Zoologica Scripta 23: 33–41.
Giani, N., C. Erséus & E. Martínez-Ansemil, 1990. Redefinition of the subterranean genus Krenedrilus Dumnicka (Oligochaeta, Tubificidae) with a redescription of K. papillatus Dumnicka, 1983 and the description of two new species. Stygologia 5: 55–65.
Giani, N., B. Sambugar, P. Rodriguez & E. Martinez-Ansemil, 2001. Oligochaetes in southern European groundwater: new records and an overview. Hydrobiologia 463: 65–74.
Giani, N., B. Sambugar, E. Martínez-Ansemil, P. Martin & R. M. Schmelz, 2011. The groundwater oligochaetes (Annelida, Clitellata) of Slovenia. Subterranean Biology 9: 84–102.
Gibert, J., 2001. Protocols for the ASsessment and Conservation of Aquatic Life in the Subsurface (PASCALIS): a European Project. Proceedings of “Mapping Subterranean Biodiversity” Special Publication, Karst Water Institute and Laboratoire souterrain de Moulis, Moulis: 19–21.
Gibert, J. & D. C. Culver, 2005. Diversity Patterns in Europe. In Culver, D. C. & W. B. White (eds), Encyclopedia of Caves. Elsevier Academic Press, New York: 196–201.
Gibert, J. & D. C. Culver, 2009. Assessing and conserving groundwater biodiversity: an introduction. Freshwater Biology 54: 639–648.
Gibert, J., D. Culver, C. Dole-Olivier, M. J. Malard, F. M. C. Christman & L. Deharveng, 2009. Assessing and conserving groundwater biodiversity: synthesis and perspectives. Freshwater Biology 54: 930–941.
Gonzalez Amuchastegui, M. J., 2000. Morphoclimatic evolution in the Basque Country during Quaternary. Cuaternario y Geomorfología 14: 79–99.
González Fernández, B., M. Meléndez Asensio, E. Menéndez Casares & M. Gutiérrez Clavero, 2005. Propuesta de declaración de Puntos de Interés Hidrogeológico en los acuíferos jurásicos de Gijón-Villaviciosa (Asturias): nacimiento del río España, nacimiento del río Peña de Francia, cueva del Lloviu y fuente de La Ruxidora. Trabajos de Geología, Universidad de Oviedo 26: 141–148.
Hahn, J. H. & A. Fuchs, 2009. Distribution patterns of groundwater communities across aquifer types in south-western Germany. Freshwater Biology 54: 848–860.
Healy, B., 1980. Records of Enchytraeidae (Oligochaeta) from Western France and the Pyrénées. Bulletin du Museum National d’Histoire Naturelle Paris Séries 4(A2): 421–443.
IBM, 2011. IBM SPSS Advanced Statistics. Armonk, IBM.
ITGE-DGOHCA, 1999. Programa de actualización del inventario hidrogeológico (PAHI) Análisis del conocimiento actual Evaluación y programación de estudios en las cuencas intercomunitarias. Instituto Tecnologico Geominero de España, Madrid.
Juberthie, C. & V. Decu, 1994. Encyclopaedia Biospeleologica. Tome I. Société de Biospéologie, Moulis (C.N.R.S.), Bucharest (Romanian Academy).
Malard, F., C. Boutin, A. I. Camacho, D. Ferreira, G. Michel, B. Sket & F. Stoch, 2009. Diversity patterns of stygobiotic crustaceans across multiple spatial scales in Europe. Freshwater Biology 54: 756–776.
Martin, P., E. Martinez-Ansemil, A. Pinder & T. Timm, 2008. Global diversity of oligochaetous clitellates (“Oligochaeta”; Clitellata) in freshwater. Hydrobiologia 595: 117–127.
Martin, P., D. De Broyer, F. Fies, G. Michel, R. Sablon & K. Wouters, 2009. Biodiversity of Belgian groundwater fauna in relation to environmental conditions. Freshwater Biology 54: 814–829.
Martínez-Ansemil, E., M. Creuzé Des Châtelliers, P. Martin & B. Sambugar, 2012. The Parvidrilidae – a diversified groundwater family: description of six new species from southern Europe, and clues for its phylogenetic position within Clitellata (Annelida). Zoological Journal of the Linnean Society 166: 530–558.
Mary, G., 1983. Evolución del margen costero de la Cordillera Cantábrica en Asturias desde el Mioceno. Trabajos de Geología, Universidad de Oviedo 13: 3–35.
Menéndez Casares, E., B. González, M. Gutiérrez Claverol & J. C. García-Ramos, 2004. Precisiones sobre los acuíferos de la cuenca jurásica asturiana (NO de España). Trabajos de Geología, Universidad de Oviedo 24: 119–126.
Michel, G., F. Malard, L. Deharveng, T. Di Lorenzo, B. Sket & C. De Broyer, 2009. Reserve selection for conserving groundwater biodiversity. Freshwater Biology 54: 861–876.
Notenboom, J., 1991. Marine regressions and the evolution of groundwater dwelling amphipods (Crustacea). Journal of Biogeography 18: 437–454.
Pinder, A. M., S. M. Eberhard & W. F. Humphreys, 2006. New phallodrilines (Annelida: Clitellata: Tubificidae) from Western Australian groundwater. Zootaxa 1304: 31–48.
Pipan, T., 2005. Epikarst – a promising habitat. Copepod fauna, its diversity and ecology: a case study from Slovenia (Europe). Založba ZRC, Ljubljana.
Pipan, T. & D. C. Culver, 2007. Regional species richness in an obligate subterranean dwelling fauna – epikarst copepods. Journal of Biogeography 34: 854–861.
Pipan, T., M. C. Christman & D. C. Culver, 2006. Dynamics of epikarst communities: microgeographic pattern and environmental determinants of epikarstic copepods in Organ Cave, West Virginia. American Midland Naturalist 156: 75–87.
Reboleira, A. S. P. S., P. A. V. Borges, F. Gonçalves, A. R. M. Serrano & P. Oromí, 2011. The subterranean fauna of a biodiversity hotspot region – Portugal: an overview and its conservation. International Journal of Speleology 40: 23–37.
Rodriguez, P., 1986a. Nuevos resultados acerca de la fauna de oligoquetos acuáticos del País Vasco y cuenca alta del Ebro 1 Haplotaxidae, Naididae y Tubificidae. Munibe Ciencias Naturales 38: 75–80.
Rodriguez, P., 1986b. Nuevos resultados acerca de la fauna de oligoquetos acuáticos del País Vasco y cuenca alta del Ebro 2 Enchytraeidae. Munibe Ciencias Naturales 38: 75–80.
Rodriguez, P. & A. Achurra, 2010. New species of aquatic oligochaetes (Annelida: Clitellata) from groundwaters in karstic areas of northern Spain, with taxonomic remarks on Lophochaeta ignota Stolc, 1886. Zootaxa 2332: 21–39.
Rodriguez, P. & J. C. Armas, 1983. Contribution à la connaissance de la faune d’Oligochetès aquatiques du pays basque et zones limitrophes. Annales de Limnologie 19: 93–100.
Rodriguez, P. & N. Giani, 1984. Description de Varichaetadrilus bizkaiensis n sp.; nouvelle espèce de Tubificidae (Oligochaeta) d’Espagne. Bulletin de la Société d’Histoire Naturelle de Toulouse 120: 127–130.
Rodriguez, P. & N. Giani, 1986. Description de trios espèces nouvelles d’Oligochètes aquatiques du Pays Basque (Espagne). Hydrobiologia 139: 269–276.
Rodriguez, P. & N. Giani, 1987. Sur deux espèces de Lumbriculidae (Oligochaeta) cavernicoles: Cookidrilus speluncaeus n gen, n sp et Trichodrilus diversisetosus Rodriguez, 1986. Bulletin de la Société d’Histoire Naturelle de Toulouse 123: 45–49.
Rodriguez, P. & N. Giani, 1989. New species of Phallodrilus (Oligochaeta, Tubificidae) from caves of northern Spain and southwestern France. Hydrobiologia 180: 57–63.
Rodriguez, P. & T. Reynoldson, 2011. The pollution biology of aquatic oligochaetes. Springer, Dordrecht.
Roskov, Y., T. Kunze, T. Orrell, L. Abucay, L. Paglinawan, A. Culham, N. Bailly., P. Kirk, T. Bourgoin, G. Baillargeon, W. Decock, A. De Wever & V. Didžiulis, 2014. Species 2000 & ITIS Catalogue of Life, 2014 Annual Ch. Digital resource at www.catalogueoflife.org/annual-checklist/2014. Species 2000: Naturalis, Leiden, the Netherlands.
Sambugar, B., N. Giani & E. Martínez-Ansemil, 1999. Groundwater oligochaetes from southern-Europe Tubificidae with marine phyletic affinities: new data with description of a new species, review and consideration on their origin. Memoires de Biospeologie XXVI: 107–116.
Serrano, E., J. J. González-Trueba, R. Pellitero, M. González-García & M. Gómez-Lende, 2013. Quaternary glacial evolution in the Central Cantabrian Mountains (Northern Spain). Geomorphology 196: 66–82.
Sket, B., 1999. The nature of biodiversity in hypogean waters and how it is endangered. Biodiversity and Conservation 8: 1319–1338.
Sket, B., 2008. Can we agree on an ecological classification of subterranean animals? Journal of Natural History 42: 1549–1563.
Stoch, F. & D. M. P. Galassi, 2010. Stygobiotic crustacean species richness: a question of numbers, a matter of scale. Hydrobiologia 653: 217–234.
Stock, J. H., 1980. Regression model evolution as exemplified by the genus Pseudoniphargus (Amphipoda). Bijdragen tot de Dierkunde 50: 105–144.
Trontelj, P., C. J. Douady, C. Fišer, J. Gibert, Š. Gorički, T. Lefébure, B. Sket & V. Zakšek, 2009. A molecular test for cryptic diversity in ground water: how large are the ranges of macro-stygobionts? Freshwater Biology 54: 727–744.
Uchupi, E., 1988. The Mesozoic–Cenozoic geologic evolution of Iberia, a tectonic link between Africa and Europe. Revista de la Sociedad Geológica de España 1: 257–294.
Zagmajster, M., D. Eme, C. Fišer, D. Galassi, P. Marmonier, F. Stoch, J. F. Cornu & F. Malard, 2014. Geographic variation in range size and beta diversity of groundwater crustaceans: insights from habitats with low thermal seasonality. Global Ecology and Biogeography 23: 1135–1145.
Acknowledgments
We are grateful to Dr. Eduardo Menéndez Casares from the University of Oviedo for helping in the field in Oviedo and for his patience to clarify to the authors the complex geology of the region; to Miguel Luis Rodriguez from IGME and Peter Smith from Matienzo Caves Group for their assessment in the selection and finding of sampling sites in Llanes and Matienzo, respectively; and to Gotzon Aranzabal from ADES, Francisco Martinez and Aitor Galarza for helping in the field. The manuscript was improved by comments of two anonymous reviewers and Diego Fontaneto. The first author had a PhD grant from the University of The Basque Country UPV/EHU (Euskerazko tesia egiteko ikerketa pertsonala prestatzeko laguntzen deialdia 2007–2011) and has currently a PostDoc position financed by the Basque Government (Programa Posdoctoral de perfeccionamiento de doctores). The study received financial support from Cátedra UNESCO (2005–2006), the Natural Park of Gorbeia (2008), the Basque Government (Department of Environment and Regional Planning of the Basque Country, 2007) and the Research-Groups project IT405-10 (Basque Government, 2010–2012).
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling editor: Diego Fontaneto
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Achurra, A., Rodriguez, P. & Reynoldson, T.B. Is the Cantabrian region of northern Spain a biodiversity hotspot for obligate groundwater fauna? The case of oligochaetes (Annelida, Clitellata). Hydrobiologia 745, 151–166 (2015). https://doi.org/10.1007/s10750-014-2101-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-014-2101-4