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Analysis of coprolites from the extinct mountain goat Myotragus balearicus

Published online by Cambridge University Press:  20 January 2017

Frido Welker ,
Elza Duijm ,
Kristiaan J. van der Gaag ,
Bas van Geel ,
Peter de Knijff ,
Jacqueline van Leeuwen ,
Dick Mol ,
Johannes van der Plicht ,
Niels Raes  and
Jelle Reumer
...Show all authors
Frido Welker
Affiliation:
Naturalis Biodiversity Center, Sylviusweg 72, 2333 BE Leiden, The Netherlands Faculty of Archaeology, Leiden University, Reuvensplaats 3, 2300 RA Leiden, The Netherlands
Elza Duijm
Affiliation:
Naturalis Biodiversity Center, Sylviusweg 72, 2333 BE Leiden, The Netherlands
Kristiaan J. van der Gaag
Affiliation:
Forensic Laboratory for DNA Research, Department of Human Genetics, Leiden University Medical Center, The Netherlands
Bas van Geel
Affiliation:
Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Science Park 904, 1090 GE Amsterdam, The Netherlands
Peter de Knijff
Affiliation:
Forensic Laboratory for DNA Research, Department of Human Genetics, Leiden University Medical Center, The Netherlands
Jacqueline van Leeuwen
Affiliation:
University of Bern, Institute of Plant Sciences, Altenbergrain 21, CH 3013, Bern, Switzerland
Dick Mol
Affiliation:
Natuurhistorisch Museum Rotterdam, Westzeedijk 345, 3015 AA, Rotterdam, The Netherlands
Johannes van der Plicht
Affiliation:
Energy and Sustainability Research Institute, Nijenborgh 4, 9747 AG, Groningen, The Netherlands
Niels Raes
Affiliation:
Naturalis Biodiversity Center, Sylviusweg 72, 2333 BE Leiden, The Netherlands
Jelle Reumer
Affiliation:
Natuurhistorisch Museum Rotterdam, Westzeedijk 345, 3015 AA, Rotterdam, The Netherlands Balearic Museum of Natural Sciences, Palma-Port de Sóller road, km 30, apartment 55, 07100 Sóller, Mallorca, Spain Department of Earth Sciences, Utrecht University, Budapestlaan 4, 3584 CD, Utrecht, The Netherlands
Barbara Gravendeel
Affiliation:
Naturalis Biodiversity Center, Sylviusweg 72, 2333 BE Leiden, The Netherlands University of Applied Sciences Leiden, J.H. Oortweg 21, 2333 CH Leiden, The Netherlands
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Abstract

Humans colonized the Balearic Islands 5–4 ka ago. They arrived in a uniquely adapted ecosystem with the Balearic mountain goat Myotragus balearicus (Bovidae, Antilopinae, Caprini) as the only large mammal. This mammal went extinct rapidly after human arrival. Several hypotheses have been proposed to explain the extinction of M. balearicus. For the present study ancient DNA analysis (Sanger sequencing, Roche-454, Ion Torrent), and pollen and macrofossil analyses were performed on preserved coprolites from M. balearicus, providing information on its diet and paleo-environment. The information retrieved shows that M. balearicus was heavily dependent on the Balearic box species Buxus balearica during at least part of the year, and that it was most probably a browser. Hindcast ecological niche modelling of B. balearica shows that local distribution of this plant species was affected by climate changes. This suggests that the extinction of M. balearicus can be related to the decline and regional extinction of a plant species that formed a major component of its diet. The vegetation change is thought to be caused by increased aridity occurring throughout the Mediterranean. Previous hypotheses relating the extinction of M. balearicus directly to the arrival of humans on the islands must therefore be adjusted.

Keywords

Ancient DNABalearic IslandsDietDNA barcodingEcological niche modelling
Type
Research Article
Information
Quaternary Research , Volume 81 , Issue 1 , January 2014 , pp. 106 - 116
Copyright
University of Washington

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References

Acevedo, P., Jiménez-Valverde, A., Lobo, J.M., and Real, R. Delimiting the geographical background in species distribution modelling. Journal of Biogeography 39, 8 (2012). 1383–1390.Google Scholar
Alcover, J.A. Disentangling the Balearic first settlement issues. ENDINS 26, (2004). 143–156.Google Scholar
Alcover, J.A. The first Mallorcans: prehistoric colonization in the Western Mediterranean. Journal of World Prehistory 21, 1 (2008). 19–84.Google Scholar
Alcover, J.A., Perez-Obiol, R., Yll, E.I., and Bover, P. The diet of Myotragus balearicus Bate 1909 (Artiodactyla: Caprinae), an extinct bovid from the Balearic Islands: evidence from coprolites. Biological Journal of the Linnean Society 66, 1 (1999). 57–74.Google Scholar
Bate, D.M.A. Preliminary note on a new artiodactyle from Mallorca Myotragus balearicus, gen. et. sp. nov. Geological Magazine 6, (1909). 385–389.Google Scholar
Bover, P. Noves aportacions al coneixement del genere Myotragus Bate 1909 (Artiodactyla, Caprinae) de les Illes Balears. (2004). Universitat de les Illes Balears, Palma de Mallorca.Google Scholar
Bover, P., and Alcover, J.A. Estimating physical characteristics of neonate Myotragus balearicus (Artiodactyla, Caprinae). Deinsea 7, (1999). 33–54.Google Scholar
Bover, P., and Alcover, J.A. The evolution and ontogeny of the dentition of Myotragus balearicus Bate, 1909 (Artiodactyla, Caprinae): evidence from new fossil data. Biological Journal of the Linnean Society 68, 3 (1999). 401–428. http://dx.doi.org/10.1111/j.1095-8312.1999.tb01178.xGoogle Scholar
Bover, P., and Alcover, J.A. Understanding Late Quaternary extinctions: the case of Myotragus balearicus (Bate, 1909). Journal of Biogeography 30, 5 (2003). 77–81.Google Scholar
Bover, P., and Alcover, J.A. Extinction of the autochthonous small mammals of Mallorca (Gymnesic Islands, Western Mediterranean) and its ecological consequences. Journal of Biogeography 35, 6 (2008). 1112–1122.CrossRefGoogle Scholar
Bover, P., Quintana, J., and Alcover, J.A. Three islands, three worlds: Paleogeography and evolution of the vertebrate fauna from the Balearic Islands. Quaternary International 182, 1 (2008). 135–144.Google Scholar
Bover, P., Quintana, J., and Alcover, J.A. A new species of Myotragus Bate, 1909 (Artiodactyla, Caprinae) from the Early Pliocene of Mallorca (Balearic Islands, western Mediterranean). Geological Magazine 147, 6 (2010). 871–885.Google Scholar
Braconnot, P., Otto-Bliesner, B., Harrison, S., Joussaume, S., Peterchmitt, J.Y., Abe-Ouchi, A., Crucifix, M., Driesschaert, E., Fichefet, T., Hewitt, C.D., Kageyama, M., Kitoh, A., Laîné, A., Loutre, M.F., Marti, O., Merkel, U., Ramstein, G., Valdes, P., Weber, S.L., Yu, Y., and Zhao, Y. Results of PMIP2 coupled simulations of the Mid-Holocene and Last Glacial Maximum — Part 1: experiments and large-scale features. Climate of the Past 3, (2007). 261–277.Google Scholar
Burjachs, F., Pérez-Obiol, R., Roure, J.M., and Julià, R. Dinámica de la vegetación durante el Holoceno en la isla de Mallorca. Mateu, I., Dupré, M., Güemes, J., and Burgaz, M.E. Trabajos de Palinología básica y aplicada. (1994). Universitat de València, Valencia. 199–201.Google Scholar
Calvo, M., and Guerrero, V.M. Los inicios de la metalurgia en las Baleares. El Calcolítico (c. 2500–1700 cal BC). (2002). Edit El Tall, Palma de Mallorca.Google Scholar
Carrión, J.S. Paleoflora y paleovegetación de la peninsula Iberica e Islas Baleares: Plioceno-Cuaternario. (2012). Minesterio de Economia y Competitividad, Madrid.Google Scholar
Cooper, A., and Poinar, H.N. Ancient DNA: do it right or not at all. Science 289, 5482 (2000). 1139 Google Scholar
Di Domenico, F., Lucchese, F., and Magri, D. Buxus in Europe: Late Quaternary dynamics and modern vulnerability. Perspectives in Plant Ecology, Evolution and Systematics 14, (2012). 354–362.Google Scholar
Doyle, J.J., and Doyle, J.L. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemistry Bulletin 19, (1987). 11–15.Google Scholar
Elith, J., Phillips, S.J., Hastie, T., Dudík, M., Chee, Y.E., and Yates, C.J. A statistical explanation of MaxEnt for ecologists. Diversity and Distributions 17, (2011). 43–57.Google Scholar
Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G., and Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25, (2005). 1965–1978.Google Scholar
Hofreiter, M., Poinar, H.N., Spaulding, W.G., Bauer, D., Martin, P.S., Possnert, G., and Pääbo, S. A molecular analysis of ground sloth diet through the last glaciations. Molecular Ecology 9, 12 (2000). 1975–1984.Google Scholar
Jenkins, D.L., Davis, L.G., Stafford, T.W., Campos, P.F., Hockett, B., Jones, G.T., Cummings, L.S., Yost, C., Connoly, T.J., Yohe, R.M., Gibbons, S.C., Raghaven, M., Rasmussen, M., Paijmans, J.L., Hofreiter, M., Kemp, B.M., Barta, J.L., Monroe, C., Gilbert, M.T., and Willerslev, E. Clovis age Western Stemmed projectile points and human coprolites at the Paisley Caves. Science 337, 6091 (2012). 223–228.Google Scholar
Jordana, X., and Köhler, M. Enamel microstructure in the fossil bovid Myotragus balearicus (Majorca, Spain): implications for life-history evolution of dwarf mammals in insular ecosystems. Palaeogeography, Palaeoclimatology, Palaeoecology 300, 1 (2011). 59–66.Google Scholar
Köhler, M., and Moyà-Solà, S. Physiological and life history strategies of a fossil large mammal in a resource-limited environment. Proceedings of the National Academy of Sciences 106, 48 (2009). 20354–20358.Google Scholar
Kopper, J.S., and Waldren, W.H. Balearic prehistory. A new perspective. Archaeology 20, 2 (1967). 108–115.Google Scholar
Krijgsman, W., Hilgen, F.J., Raffi, I., Sierro, F.J., and Wilson, D.S. Chronology, causes and progression of the Messinian salinity crisis. Nature 400, 2001 (1999). 652–655.Google Scholar
Lalueza-Fox, C., Bertranpetit, J., Alcover, J.A., Shailer, N., and Hagelberg, E. Mitochondrial DNA from Myotragus balearicus, an extinct bovid from the Balearic Islands. Journal of Experimental Zoology 288, 1 (2000). 56–62.Google Scholar
Lalueza-Fox, C., Shapiro, B., Bover, P., Alcover, J.A., and Bertranpetit, J. Molecular phylogeny and evolution of the extinct bovid Myotragus balearicus. Molecular Phylogenetics and Evolution 25, 3 (2002). 501–510.Google Scholar
Lalueza-Fox, C., Castresana, J., Sampietro, L., Marqués-Bonet, T., Alcover, J.A., and Bertranpetit, J. Molecular dating of caprines using ancient DNA sequences of Myotragus balearicus, en extinct endemic Balearic mammal. BMC Evolutionary Biology 5, (2005). 70 http://dx.doi.org/10.1186/1471-2148-5-70Google Scholar
Lázaro, A., and Traveset, A. Reproductive success of the endangered shrub Buxus balearica Lam. (Buxaceae): pollen limitation, and inbreeding, and outbreeding depression. Plant Systematics and Evolution 261, (2006). 117–128.Google Scholar
Lázaro, A., Traveset, A., and Méndez, M. Masting in Buxus balearica: assessing fruiting patterns and processes at a large spatial scale. OIKOS 115, (2006). 229–240.Google Scholar
Lobo, J.M., Jimenez-Valverde, A., and Real, R. AUC: a misleading measure of the performance of predictive distribution models. Global Ecology and Biogeography 17, (2008). 145–151.Google Scholar
Lull, V., Micó, R., Rihuette, C., and Risch, R. La Cova des Càrritx y la Cova des Mussol. Ideología y Sociedad en la Prehistoria de Menorca. (1999). Consell Insular de Menorca, Menorca.Google Scholar
MacPhee, R.D.E., and Marx, P.A. The 40.000 year plague: humans, hyperdisease and first-contact extinctions. Goodman, S.M., and Patterson, B.D. Natural Change and Human Impact in Madagascar. (1997). Smithsonian Institution Press, Washington. 169–217.Google Scholar
Magny, M., Miramont, C., and Silvan, O. Assessment of the impact of climate and anthropogenic factors on Holocene Mediterranean vegetation in Europe on the basis of palaeohydrological records. Palaeogeography, Palaeoclimatology, Palaeoecology 186, 1/2 (2002). 255–290.Google Scholar
Martin, P.S. Prehistoric overkill: the global model. Martin, P.S., and Klein, R.G. Quaternary Extinctions. A Prehistoric Revolution. (1984). University of Arizona Press, Tucson. 354–403.Google Scholar
Moyà-Solà, S., Köhler, M., Alba, D., and Pons-Moyà, J. El significado de Myotragus batei y M. binigasensis en la evolución del género Myotragus (Bovidae, Mammalia) en la islas Baleares. Pons, G.X., and Vicens, D. Geomorfologia litoral I Quaternari. Homenatge a Joan Cuerda Barceló. Monografies de la Societat d'Historia Natural de les Balears 14, (2007). Universitat de Valencia, Valencia. 155–180.Google Scholar
Navarro-Cerrillo, R.M., Hernández-Bermejo, J.E., and Hernández-Clemente, R. Evaluating models to assess the distribution of Buxus balearica in southern Spain. Applied Vegetation Science 14, (2011). 256–267.Google Scholar
Ninyerola, M., Sáez, L., and Pérez-Obiol, R. Relating postglacial relict plants and Holocene vegetation dynamics in the Balearic Islands through field surveys, pollen analysis and GIS modelling. Plant Biosystems 141, 3 (2007). 292–304.Google Scholar
Pääbo, S., Poinar, H., Serre, D., Jaenicke-Després, V., Hebler, J., Rohland, N., Kuch, M., Krause, J., Vigilant, L., and Hofreiter, M. Genetic analysis from ancient DNA. Annual Review of Genetics 38, (2000). 645–679.Google Scholar
Palmer, M., Pons, G.X., Cambefort, I., and Alcover, J.A. Historical processes and environmental factors as determinants of inter-island differences in endemic faunas: the case of the Balearic Islands. Journal of Biogeography 26, 4 (1999). 813–823.Google Scholar
Palombo, M.R., Bover, P., Valli, A.M.F., and Alcover, J.A. The Plio-Pleistocene endemic bovids from the Western Mediterranean islands: knowledge, problems and perspectives. Hellenic Journal of Geosciences 41, (2008). 153–162.Google Scholar
Palombo, M.R., Rozzi, R., and Bover, P. The endemic bovids from Sardinia and the Balearic Islands: the state of the art. Geobios 46, (2013). 127–142.Google Scholar
Patton, M. Blitzkrieg or Sitzkrieg: the extinction of endemic faunas in Mediterranean island prehistory. Nicholson, R.A., and O' Connor, T.P. People as an Agent of Environmental Change. (2000). Oxbow Books, Oxford. 117–124.Google Scholar
Pérez-Obiol, R., and Sadori, L. Similarities and dissimilarities: synchronisms and diachronisms in the Holocene vegetation history of the Balearic Islands and Sicily. Vegetation History and Archaeobotany 16, 4 (2007). 259–265.Google Scholar
Peterson, A.T., Soberón, J., Pearson, R.G., Anderson, R.P., Martínez-Meyer, E., Nakamura, M., and Araújo, M.B. Ecological Niches and Geographic Distributions. (2011). Princeton University Press, Princeton and Oxford.Google Scholar
Phillips, S.J., Anderson, R.P., and Schapire, R.E. Maximum entropy modeling of species geographic distributions. Ecological Modelling 190, (2006). 231–259.CrossRefGoogle Scholar
Poinar, H.N., Hofreiter, M., Spaulding, W.G., Martin, P.S., Stankiewicz, B.A., Bland, H., Evershed, R.P., Possnert, G., and Paabo, S. Molecular coproscopy: dung and diet of the extinct ground sloth Nothrotherops shastensis. Science 281, 5375 (1998). 402–406.Google Scholar
Quintana, J., Kohler, M., and Moya-Sola, S. Nuralagus rex, gen. et sp. nov, an endemic insular giant rabbit from the Neogene of Minorca (Balearic Islands, Spain). Journal of Vertebrate Paleontology 31, 2 (2011). 231–240.Google Scholar
Raes, N. Partial versus full species distribution models. Natureza & Conservação 10, (2012). 127–138.Google Scholar
Raes, N., and ter Steege, H. A null-model for significance testing of presence-only species distribution models. Ecography 30, (2007). 727–736.Google Scholar
Ramirez, O., Gigli, E., Bover, P., Alcover, J.A., Bertranpetit, J., Castresana, J., and Lalueza-Fox, C. Paleogenomics in a temperate environment: shotgun sequencing from an extinct Mediterranean Caprine. Publich Library of Science One 4, 5 (2009). e5670 http://dx.doi.org/10.1371/journal.pone.0005670Google Scholar
Ramis, D., and Bover, P. A review of the evidence for domestication of Myotragus balearicus Bate 1909 (Artiodactyla, Caprinae) in the Balearic Islands. Journal of Archaeological Science 28, 3 (2001). 265–282.Google Scholar
Ramis, D., Alcover, J.A., Coll, J., and Trias, M. The chronology of the first settlement of the Balearic Islands. Journal of Mediterranean Archaeology 15, 1 (2002). 3–24.Google Scholar
Rohland, N., and Hofreiter, M. Ancient DNA extraction from bones and teeth. Nature Protocols 2, (2007). 1756–1762.Google Scholar
Sánchez-Fernández, D., Lobo, J.M., and Hernández-Manrique, O.L. Species distribution models that do not incorporate global data misrepresent potential distributions: a case study using Iberian diving beetles. Diversity and Distributions 17, (2011). 163–171.Google Scholar
Savolainen, V., Fay, M.F., Albach, D.C., Backlund, A., van der Bank, M., Cameron, K.M., Johnson, S.A., Lledó, M.D., Pintaud, J.C., Powell, M., Sheahan, M.C., Soltis, D.E., Soltis, P.S., Weston, P., Whitten, W.M., Wurdack, K.J., and Chase, M.W. Phylogeny of the eudicots: a nearly complete familial analysis based on rbcL gene sequences. Kew Bulletin 55, (2000). 257–309.Google Scholar
Schlumbaum, A., Tensen, M., and Jaenicke-Després, V. Ancient plant DNA in archaeobotany. Vegetation History and Archaeobotany 17, 2 (2008). 233–244.Google Scholar
van der Geer, A., Lyras, G., de Vos, J., and Dermitzakis, M. Evolution of Island Mammals. Adaptation and Extinction of Placental Mammals on Islands. (2010). Wiley-Blackwell, Chichester.Google Scholar
Waldren, W.H. Balearic prehistoric ecology and culture. The excavation of certain caves, rock shelters and settlements. BAR International Series 149, (1982). Archaeopress, Oxford.Google Scholar
Waldren, W.H., Ensenyat, J., and Orvay, J. New coals on old fires: the question of early Balearic settlement. Waldren, W.H., and Ensenyat, J.A. World Islands in Prehistory: International Insular Investigations: V Deia International Conference of Prehistory. BAR International Series 1095, (2002). Archaeopress, Oxford. 68–90.Google Scholar
White, T.J., Bruns, T., Lee, S., and Taylor, J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Innis, M.A., Gelfand, D.H., and Sninsky, J.J. PCR Protocols, A Guide to Methods and Applications. (1990). Academic Press, San Diego. 315–322.Google Scholar
Winkler, D.E. Dentition and Diet: New 3D-Methods help to discover Dental Adaptations in the Extinct Bovid Myotragus. MSc Thesis (2010). Hamburg University, Hamburg.Google Scholar
Winkler, D.E., Schulz, E., Calandra, I., Gailer, J.P., Landwehr, C., and Kaiser, T.M. Indications for a dietary change in the extinct Bovid genus Myotragus (Plio-Holocene, Mallorca, Spain). Geobios 46, (2013). 143–150.Google Scholar
Withers, P.C. Comparative Animal Physiology. (1992). Saunders, London.Google Scholar
Yll, E.I., Perez-Obiol, R., and Juliá, R. Vegetational change in the Balearic Islands (Spain) during the Holocene. Historical Biology 9, 1/2 (1994). 83–89.Google Scholar
Yll, E.I., Perez-Obiol, R., Pantaleon-Cano, J., and Roure, J. Palynological evidence for climatic change and human activity during the Holocene on Minorca (Balearic Islands). Quaternary Research 48, 3 (1997). 339–347.Google Scholar