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Mammalian Biology

, Volume 78, Issue 6, pp 430–437 | Cite as

Dietary divergence in space and time – Lessons from the dwarf–goat Myotragus balearicus (Pleisto-Holocene, Mallorca, Spain)

  • Daniela E. WinklerEmail author
  • Lars W. van den HoekOstende
  • Ellen Schulz
  • Ivan Calandra
  • Juan-Pablo Gailer
  • Christina Landwehr
  • Thomas M. Kaiser
Original Investigation

Abstract

Newly colonised, isolated habitats, like islands, provide diverse niches to be filled and are prone to facilitate ecological separation which might lead to an adaptive radiation. Examples of such radiations can be found in the Mediterranean for the genera Candiacervus (Crete), Nesogoral (Sardinia) and Hoplitomeryx (Gargano). A different strategy to cope with limited resources on islands is generalism. We test whether populations of the endemic bovid Myotragus balearicus from two sites and Pleistocene as well as Holocene levels on Mallorca island displays ecological separation indicated by diet, or whether the species shifted its dietary trait towards generalism. We expect to find either: (1) dietary divergence in space and time (between sites and stratigraphic levels), which would indicate niche partitioning and/or a shift in dietary traits due to environmental influences; or (2) dietary congruence in a less specialised, generalistic dietary strategy in space and time which would indicate a flexible trait to cope with instable resource availability. We compare individuals from a fossil assemblage at a northern site and one assemblage from the eastern coast in terms of their dietary traits. Traits are reconstructed using dental dietary proxies, complementary in time scale and resolution. (1) 3D-dental topometry and (2) enamel surface texture analysis. Data suggest that individuals from both assemblages of M. balearicus behaved as variable browse dominated intermediate feeders. We thus conclude that the observed variability relates to a shift towards generalism as a subsistence strategy. We consider hypsodonty the pre-adaptation for this life style that enabled M. balearicus to exploit almost any food source in its energetically restricted island habitat.

Keywords

Bovids Island evolution Surface texture Diet Tooth morphology 

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References

  1. Alcover, J.A., 1976. L’evoluciónde Myotragus Bate 1909(Artiodactyla, Rupicaprini), un procés biologic lligat al fenómen de la insularitat. Butlletí de la Institució Catalana d’História Natural. Sec. Geol. 40 (1), 59–94.Google Scholar
  2. Alcover, J.A., Moyá-Solá, S., Pons-Moyá, J., 1981. Chimeras of the Past (Translated from Catalan). (Editorial Moll, Palma de Mallorca, Spain), vol. 1. Monografies Científiques, pp. 1–260.Google Scholar
  3. Alcover, J.A., Perez-Obiol, R., Yll, E.-I., Bover, P., 1999. The diet of Myotragus balearicus Bate 1909 (Artiodactyla, Caprinae), an extinct bovid from the Balearic Islands, evidence from coprolites. Biol. J. Linn. Soc. 66 (1), 57–74.Google Scholar
  4. Archer, D., Sanson, G., 2002. Form and function of the selenodont molar in southern African ruminants in relation to their feeding habits. J. Zool. (Lond) 257, 13–26.CrossRefGoogle Scholar
  5. Bover, P., Alcover, J.A., 1999. The evolution and ontogeny of the dentition of Myotragus balearicus Bate, 1909 (Artiodactyla, Caprinae): evidence from new fossil data. Biol. J. Linn. Soc. 68 (3), 401–428.CrossRefGoogle Scholar
  6. Bover, P., Quintana, J., Alcover, J.A., 2010. A new species of Myotragus Bate, 1909 (Artiodactyla, Caprinae) from the early Pliocene of Mallorca (Balearic Islands, western Mediterranean). Geol. Mag. 147, 871–885.CrossRefGoogle Scholar
  7. Butler, M., 1980. The giant erinaceid insectivore, Deinogalerix Freudenthal, from the upper Miocene of Gargano, Italy. Scr. Geol. 57, 1–72.Google Scholar
  8. Calandra, I., 2011. Tribology of dental enamel facets of Ungulates and Primates (Mammalia), Tracing tooth-food interaction through 3D enamel microtexture analyses, Unpublished Ph.D. Thesis. University of Hamburg.Google Scholar
  9. Calandra, I., Schulz, E., Kaiser, T.M., 2012. Teasing apart the contribution of hard items on 3D dental microtextures in primates. J. Hum. Evol.,  https://doi.org/10.1016/jjhevol.2012.05.001.
  10. Cliff, N., 1996. Ordinal Methods for Behavioral Data Analysis. Lawrence Erlbaum, Mahawah, New Jersey.Google Scholar
  11. Damuth, J., Janis, CM., 2011. On the relationship between hypsodonty and feeding ecology in ungulate mammals, and its utility in palaeoecology. Biol. Rev. 86, 733–758.PubMedCrossRefPubMedCentralGoogle Scholar
  12. Darwin, F., 1909. The Foundations of the Origin of Species, Two Essays Written in 1842 and 1844 by Charles Darwin. Cambridge Univ. Press, Cambridge, UK.Google Scholar
  13. De Vos, J., 1979. The endemic Pleistocene deer of Crete. Proceedings of the Konin-klijke Nederlandse Akademie van Wetenschappen, Series B 82 (1), 59–90.Google Scholar
  14. De Vos, J., 1984. The endemic Pleistocene deer of Crete, 31. Verhandeling der Koninklijke Nederlandse Akademie van Wetenschappen, AfdelingNatuurkunde, Eerste Reeks, pp. 1–100.Google Scholar
  15. De Vos, J., Van derGeer, A.A.E., 2002. Major patterns and processes in biodiversity, axonomic diversity on islands explained in terms of sympatric speciation. In: Waldren, B., Ensenyat (Eds.), World Islands in Prehistory, International Insular Investigations, 1095. VDeia International Conference of Prehistory. Bar International Series, pp. 395–405.Google Scholar
  16. Duggen, S., Hoernle, K., van den Bogaard, P., Rupke, L, Morgan, J.P., 2003. Deep roots of the Messinian salinity crisis. Nature 422 (6932), 602–606.PubMedCrossRefGoogle Scholar
  17. Dunnett, C.W., 1980. Pairwise multiple comparisons in the unequal variance case. J. Am. Stat. Assoc. 75 (372), 796–800.CrossRefGoogle Scholar
  18. Feranec, R.S., 2003. Stable isotopes, hypsodonty, and the paleodiet of Hemiauche-nia Mammalia: Camelidae): a morphological specialization creating ecological generalization. Paleobiology 29 (2), 230–242.CrossRefGoogle Scholar
  19. Freudenthal, M., 1976. Rodent stratigraphy of some Miocene fissures in Gargano (prov. Foggia, Italy). Scr. Geol. 37, 1–23.Google Scholar
  20. Freudenthal, M., Martín-Suarez, E., 2006. Gliridae (Rodentia, Mammalia) from the late miocene fissure Filling Biancone 1 (Gargano, Province of Foggia, Italy). Palaeontol. Electron. 9 (2), 1–23.Google Scholar
  21. Gailer, J.P., Kaiser, T.M., 2010. Quantifying chewing efficiency of ruminant dental patterns - an approach using three-dimensional metrology systems. 80. Jahrestagung der Paläontologischen Gesellschaft, München, Germany. Zitteliana B29, 38.Google Scholar
  22. Heywood, J.J.N., 2009. Functional anatomy of bovid upper molar occlusal surfaces with respect to diet. J. Zool. 281 (1), 1–11.CrossRefGoogle Scholar
  23. International Organization for Standardization, 2012. ISO 25178-2 - Geometrical Product Specifications (GPS) - Surface Texture, Areal - Part 2: Terms Definitions and Surface Texture Parameters.Google Scholar
  24. Jordana, X., Marin-Moratalla, N., DeMiguel, D., Kaiser, T.M., Köhler, M., 2012. Evidence of correlated evolution of hypsodonty and exceptional longevity in endemic insular mammals. Proc. R. Soc. B 279 (1741), 3339–3346.CrossRefGoogle Scholar
  25. Köhler, M., Moyà-Solà, S., 2001. Phalangeal adaptations in the fossil insular goat Myotragus. J. Vert. Paleontol. 21 (3), 621–624.CrossRefGoogle Scholar
  26. Köhler, M., Moyà-Solà, S., 2004. Reduction of brain size and sense organs in the fossil insular bovid Myotragus. Brain Behav. Evol. 63, 125–140.Google Scholar
  27. Krijgsman, W., Hilgen, F.J., Raffi, I., Sierro, F.J., Wilson, D.S., 1999. Chronology, causes and progression of the Messinian salinity crisis. Nature 400, 652–655.CrossRefGoogle Scholar
  28. Leinders, J.J.M., 1984. Hoplitomerycidae fa. nov. (Ruminantia, Mammalia) from Neogene fissure fillings in Gargano (Italy); part 1: The cranial osteology of Hoplit-omeryxgen. nov. and a discussion on the classification of pecoran families. Scr. Geol. 70, 1–51.Google Scholar
  29. Locatelli, E., Due, R.A., van den Bergh, G.B., van den Hoek Ostende, L.W., 2012. Pleistocene survivors and Holocene extinctions: the giant rats from Liang Bua(Flores, Indonesia). Quatern. Int. 281, 47–57.CrossRefGoogle Scholar
  30. Marcus, L.F., 1999. Variation in selected skeletal elements of the fossil remains of Myotragus balearicus, a Pleistocene bovid from Mallorca. Acta Zool. Acad. Sci. Hung. 44 (1/2), 113–137.Google Scholar
  31. Mayr, E., 1963. Animal Species and Evoluti. Belknap Press, Cambridge, MA. Mazza, P.P.A., Rustioni, M., 2011. Five new species of Hoplitomeryx from the Neogene of Abruzzo and Apulia (central and southern Italy) with revision of the genus and of Hoplitomeryx matthei Leinders, 1983. Zool. J. Linn. Soc. 163, 1304–1333.Google Scholar
  32. Moya-Solà, S., Pons Moyà, S., 1979. J. Catálogo de los yacimientos con fauna de ver-tebrados del Plioceno, Cuaternario y Holoceno de las Baleares, Endin, 6/7., pp. 59–74.Google Scholar
  33. Nieberg, C, Gailer, J.P., Kaiser, T.M., 2009. Quantifying functional traits in the ungulate dentition. In: 79. Jahrestagung der Paläontologischen Gesellschaft, 5–7, Oktober 2009, vol. 3, Bonn, Germany, Terra Nostra, p. 83.Google Scholar
  34. Nieberg, C, Schwitzer, S., Kaiser, T.M., 2010. Quantifying occlusal Topometry and complexity in non-ruminating mammals. 80. Jahrestagung der Paläontologischen Gesellschaft, München, Germany. Zitteliana B29, 78.Google Scholar
  35. Ninyerola, M., Sáez, L., Pérez-Obiol, R., 2007. Relating postglacial relict plants and Holocene vegetation dynamics in the Balearic Islands through field surveys, pollen analysis and GIS modeling. Plant Biosyst. 141, 292–304.CrossRefGoogle Scholar
  36. Palombo, M.R., Bover, P., Valli, A.F.M., Alcover, J.A., 2006. The Plio-Pleistocene endemic bovids from the Western Mediterranean islands, knowledge, problems and perspectives. Hell. J. Geosci. 41, 153–162.Google Scholar
  37. Palombo, M.R., Rozzi, R., Bover, P., 2013. The endemic bovids from Sardinia and the Balearic Islands: state ofthe art. Geobios 46 (1/2), 127–142.CrossRefGoogle Scholar
  38. Pérez-Obiol, R., Yll, E.I., Pantaleón Cano, J., Roure, J.M., 2000. Evaluación de los impactos antrópicos y los cambios climáticos en el paisaje vegetal de las islas Baleares durante los últimos 8000 anos. In: Guerrero, V.M., Gornés, S. (Eds.), Colonización humana en ambientes insulares. Interacción con el medio y adaptación cultural. Palma de Mallorca, Universitat de les Illes Balears, pp. 444–454.Google Scholar
  39. Development Core Team, R., 2011. R, A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-900051-07-0, http://www.R-project.org.Google Scholar
  40. Rozzi, R., Palombo, M.R., 2013. Lights and shadows in the evolutionary patterns of insular bovids. Int. Zool.,  https://doi.org/10.1111/1749-4877.12055.PubMedCrossRefPubMedCentralGoogle Scholar
  41. Schmidt-Kittler, N., 1984. Pattern analysis of occlusal surfaces in hypsodont herbivores and its bearing on morpho-functional studies. Proc. Konink. Nederl. Akad. Wetensch. Ser. B 87 (4), 453–480.Google Scholar
  42. Schulz, E., Calandra, I., Kaiser, T.M., 2010. Applying tribology to teeth of hoofed mammals. Scanning 32, 162–182.PubMedCrossRefPubMedCentralGoogle Scholar
  43. Schulz, E., Piotrowski, V., Clauss, M., Merceron, G., Kaiser, T.M., 2013a. The effect of abrasive silica particles on tooth wear of Oryctolagus cuniculus (Lagomorpha). PLoS ONE 8 (2), e56167.PubMedPubMedCentralCrossRefGoogle Scholar
  44. Schulz, E., Calandra, I., Kaiser, T.M., 2013b. Feeding ecology and chewing mechanics in hoofed mammals: 3D tribology of enamel wear. Wear 300 (1/2), 169–179.CrossRefGoogle Scholar
  45. Scott, J.R., Godfrey, L.R., Jungers, W.L., Scott, R.S., Simons, E.L., Teaford, M.F., Ungar, P.S., Walker, A., 2009. Dental microwear texture analysis of two families of subfossil lemurs from Madagascar. J. Hum. Evol. 56, 405–416.PubMedCrossRefPubMedCentralGoogle Scholar
  46. Scott, R.S., Ungar, P.S., Bergstrom, T.S., Brown, C.A., Grine, F.E., Teaford, M.F., Walker, A., 2005. Dental microweartexture analysis reflects diets of living primates and fossil hominins. Nature 436, 693–695.PubMedCrossRefPubMedCentralGoogle Scholar
  47. Shaw, K.L., 2002. Conflict between nuclear and mitochondrial DNA phylogenies of a recent species radiation, what mtDNA reveals and conceals about modes of speciation in Hawaiian crickets. Proc. Nat. Acad. Sci. U.S.A. 99, 16122–16127.CrossRefGoogle Scholar
  48. Sondaar, P.Y., 1977. Insularity and its effects on mammal evolution. In: Hecht, M.K., Goody, P.C., Hecht, B.M. (Eds.), Major Patterns in Vertebrate Evolution. Plenum Publishing Corporation, New York, pp. 671–707.CrossRefGoogle Scholar
  49. Van derGeer, A.A.E., 2005. The postcranial ofthe deer Hoplitomeryx (Mio-Pliocene; Italy), another example of adaptive radiation on Eastern Mediterranean Islands. Monografies de la Societat d’Història Natural de les Balears, 12., pp. 325–336.Google Scholar
  50. Van derGeer, A.A.E., Dermitzakis, M., De Vos, J., 2006. Crete before the Cretans, the reign of dwarfs. Pharos 13, 121–132.Google Scholar
  51. Van der Geer, A.A.E., 2008. The effect of insularity on the Eastern Mediterranean early cervoid Hoplitomeryx, the study ofthe forelimb. Quatern. Int. 182 (1), 145–159.CrossRefGoogle Scholar
  52. Villier, B., Van den HoekOstende, L.W., De Vos, J., 2013. New discoveries of the giant hedgehog Deinogalerix from the Miocene of Gargano (Apulia, Italy). Geobios 46 (1/2), 63–75.CrossRefGoogle Scholar
  53. Wilcox, R.R., 2003. Applying Contemporary Statistical Techniques. Academic Press, San Diego, CA.Google Scholar
  54. Wilcox, R.R., 2005. Introduction to Robust Estimation and Hypothesis Testing, 2nd ed. Elsevier Academic Press, London.Google Scholar
  55. Winkler, D.E., Schulz, E., Calandra, I., Gailer, J.P., Landwehr, C, Kaiser, T.M., 2013. Indications for a dietary change in the extinct Bovid genus Myotragus (Plio-Holocene, Mallorca, Spain). Geobios 46 (1/2), 143–150.CrossRefGoogle Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2013

Authors and Affiliations

  • Daniela E. Winkler
    • 1
    Email author
  • Lars W. van den HoekOstende
    • 2
  • Ellen Schulz
    • 1
  • Ivan Calandra
    • 3
  • Juan-Pablo Gailer
    • 1
  • Christina Landwehr
    • 1
  • Thomas M. Kaiser
    • 1
  1. 1.Biocenter Grindel & Zoological MuseumUniversity of HamburgHamburgGermany
  2. 2.Netherlands Centre for Biodiversity NaturalisCR LeidenThe Netherlands
  3. 3.Université de Bourgogne, BiogéosciencesDijonFrance

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