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Tooth Morphology in Fossil and Extant Lagomorpha (Mammalia) Reflects Different Mastication Patterns

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Abstract

The functional interpretation of the cheek teeth and the mastication cycle of Lagomorpha are deduced from various aspects of tooth morphology of fossil and extant species. Mastication is composed of an almost orthal shearing and transverse grinding in a lingual direction. Shearing blades are not only indicated by facets but as well by thickened enamel. A primary shearing blade (PSB) inherited from stem lagomorphs occurs in all examined species. It can be correlated with facets 1 and 5 (sensu Crompton 1971) and occurs in very few mammals; it is conspicuously absent in the sister-taxon Rodentia. A secondary shearing blade (SSB) occurs in derived Ochotonidae and two basal Leporidae (Romerolagus and Pronolagus) as a convergent pattern. In fossil ochotonids from Europe, the “lagicone structure” is gradually reduced in favor of the SSB. Thus, ochotonids strengthen the shearing ability, whereas most leporids favor the grinding function realized by the partial crenulation of the enamel band of the re-entrant folds. For the mastication cycle, the distinct phases were recognized, related to phase I of the tribosphenic model. The first movement (phase Ia) is directed almost orthally, the second (phase Ib) lingually. Only in Lepus europaeus was an additional phase detected, which might correspond to phase II.

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Abbreviations

BSPG:

Bayerische Staatssammlung für Paläontologie und Geologie, München, Germany

KOE:

Collection of teeth and samples for enamel investigation at the Steinmann-Institut, Universität Bonn, Germany

MB:

Museum für Naturkunde, Berlin, Germany

Naturalis:

Museum Naturalis, Leiden, The Netherlands

NHMB:

Natural History Museum, Basel, Switzerland

SMNS:

Staatliches Museum für Naturkunde Stuttgart, Germany

STIPB:

Mammal collection at the Steinmann-Institut, Universität Bonn, Germany

ZFMK:

Zoologisches Forschungsinstitut und Museum Koenig, Bonn, Germany

ZMA:

Zoological Museum, Amsterdam, The Netherlands

char.:

characters listed in Appendix

EDJ:

enamel dentine junction

GS:

grinding surface

HSB:

Hunter-Schreger Bands

IRRE:

irregular enamel

LCS:

lagicone structure

OES:

outer enamel surface

P–M:

upper premolars and molars

p–m:

lower premolars and molars

PSB:

primary shearing blade

RE:

radial enamel

REF:

re-entrant fold (= internal hypsotria, hypoflexus)

SSB:

secondary shearing blade (ochotonid SSB)

(SSB):

composed secondary shearing blade

TDF:

touch down facet

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Acknowledgments

This research was supported by the “Deutsche Forschungsgemeinschaft” (DFG, German Research Foundation) and is publication no. 8 of the DFG Research Unit 771 “Function and performance enhancement in the mammalian dentition - phylogenetic and ontogenetic impact on the masticatory apparatus”. Many thanks to all people who made material available: Loїc Costeur (Basel), Rainer Hutterer (Bonn), David F. Mayhew (Leiden), Pierre Mein (Lyon), Doris Mörike (Stuttgart), Gertrud Rößner (Munich), Danilo Torre (Firenze), Wilma Wessels (Utrecht), and Reinhard Ziegler (Stuttgart). For comments and valuable hints: Renate Angermann (Berlin), Margarita Erbajeva (Uland-Ude), Mary Dawson (Pittsburgh), and John Wible (Pittsburgh). For technical support we thank Olaf Dülfer, Peter Göddertz, and Georg Oleschinski (all Bonn). We also would like to thank the anonymous reviewers for helpful comments which served to improve the manuscript.

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  1. Steinmann-Institut für Geologie, Mineralogie und Paläontologie, Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn, Germany

    Wighart von Koenigswald, Ulrike Anders, Sandra Engels, Julia A. Schultz & Irina Ruf

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  1. Wighart von Koenigswald
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Correspondence to Wighart von Koenigswald.

Appendices

Appendix

Materials studied

Palaeolagidae

  1. 1.

    Palaeolagus sp. (most probably Palaeolagus temnodon Douglass, 1901)—rich material of upper and lower jaws, late Eocene/early Oligocene, Toadstool Park Area, Nebraska, USA (col. K. Hirsch; KOE 668) [CT scans of upper and lower jaw fragments each with resolution = 0.02102 mm, CT scans of 1 upper and 1 lower cheek tooth each with resolution = 0.01232 mm].

Leporidae

  1. 2.

    Bunolagus monticularis Thomas, 1929—crania and mandibles, recent, Cape Province, South Africa (ZMA 3076, 3077).

  2. 3.

    Hypolagus brachygnathus (Petényi, 1864)—several isolated teeth, Pliocene, Rembielice, Poland (KOE 120, 1062).

  3. 4.

    Lepus europaeus Pallas, 1778—several mandibles and crania, recent, Sigmaringen, SW Germany (KOE 30, STIPB M 1162, M 1167, M 1174, M 11 84). [CT scans M1dex, m1dex (M 1162), each with resolution = 0.01943 mm.]

  4. 5.

    Lepus europaeus Pallas, 1778—several mandibles and crania, recent, Bonn, Germany (STIPB M 1170–1184).

  5. 6.

    Lepus timidus Linnaeus, 1758—cranium and mandible, recent, Faulherrnalpen, Berner Oberland, Switzerland (ZFMK 1316).

  6. 7.

    Lepus timidus Linnaeus, 1758—cranium and mandible, recent, St. Petersburg, Russia (ZFMK, 24).

  7. 8.

    Lepus timidus Linnaeus, 1758—cranium and mandible, recent, Nowosibirskaja, Russia (ZFNK 87.792).

  8. 9.

    Lepus timidus varronis Miller, 1901—cranium and mandible, recent, Gurnigel, Switzerland (ZFMK, 39.124).

  9. 10.

    Nesolagus netscheri Schlegel, 1880—cranium and mandible, recent, South Sumatra, Indonesia (Naturalis 3741)

  10. 11.

    Oryctolagus cuniculus (Linnaeus, 1758)—several crania and jaws, recent, Bonn, Germany (STIPB M6248–M6255).

  11. 12.

    Oryctolagus cuniculus (Linnaeus, 1758)—crania and mandibles, recent (domesticated) Bonn, Germany (STIPB M 3274, M3275; KOE 4099).

  12. 13.

    Oryctolagus cuniculus (Linnaeus, 1758)—cranium and mandible, recent, Tübingen, Germany (STIPB M 1190).

  13. 14.

    Poelagus majorita St. Leger, 1929, skull, recent, South Sudan, (SMNS 28732) [CT scan resolution = 0.05785 mm.]

  14. 15.

    Pronolagus rupestris (Smith, 1834)—cranium and mandible, recent, Namibia (SMNS 38755)

  15. 16.

    Pronolagus cf. rupestris (Smith, 1834)—cranium and mandible, recent, Chamis, Namaland, Namibia (MB 82038) [CT scan 0.08887 mm]

  16. 17.

    Pronolagus cf. rupestris (Smith, 1834)—cranium and mandible, recent, Churutabis, Namibia (MB 82039) [P4 sin. CT scan resolution = 0.01597 mm]

  17. 18.

    Pronolagus crassicaudatus (Geoffroy, 1832)—cranium, recent, Kasama, Zambia (MB 82036)

  18. 19.

    Pronolagus crassicaudatus (Geoffroy, 1832)—crania and mandibles, recent, Cape Province, South Africa (MB 1037 and ZMA 1317, 4020)

  19. 20.

    Pronolagus randensis Jameson, 1907—cranium and mandible, recent, Birkenfeld, Namibia (ZFMK, 56.581) [CT scan of p4 sin resolution = 0.01597 mm]

  20. 21.

    Romerolagus diazi—cranium and mandible, recent, Mexico (NHMB 10977) [CT scan of upper dentition resolution = 0.03952 mm, virtual resolution = 0.01976 mm]

  21. 22.

    Sylvilagus audubonii (Baird, 1858)—several fragmented skulls, recent,Wyoming, USA (KOE 1052, STIPB M 1159)

  22. 23.

    Sylvilagus audubonii—1 upper and 1 lower cheek tooth, recent, Wyoming, USA (M 1159 and KOE 4078), [CT scans each with resolution = 0.00751 mm]

  23. 24.

    Sylvilagus bachmani (Waterhouse, 1839)—cranium and mandibles, recent, California, USA (SMNS 17673)

  24. 25.

    Sylvilagus floridanus (Allen, 1890)—cranium and mandible, recent, Noxubee, Mississippi, USA (SMNS 45545)

Ochotonidae

  1. 26.

    Amphilagus antiquus Pomel, 1853—several mandibles and maxillae, latest Oligocene MP 30, Coderet-Branssat, France, (NMB–BST 255, 259, 268, 232,233, 234, 236, Cod 377 [CT scan resolution = 0.0154 mm, virtual resolution = 0.0077 mm], 384, 4513a, 4513c [CT scan resolution = 0.0154 mm, virtual resolution = 0.0077 mm], 4514a, 4514d)

  2. 27.

    Austrolagomys unexpectatus Stromer, 1926—cranium (type), Miocene, Elisabethfeld, Namibia (BSPG 1926X14)

  3. 28.

    Lagopsis sp.—several mandibles, middle Miocene MN 5, Steinberg bei Nördlingen, SW Germany (SMNS no number and KOE 4079) [CT scans each with 0.00961 mm, virtual resolution = 0.0048 mm]

  4. 29.

    Ochotona alpina (Pallas, 1773)—cranium and mandible, recent, Kenho, Dsingan, China (MB. 100483 [CT scans each with resolution = 0.00871 mm, virtual resolution = 0.00436 mm], 100484, 104085, 100486, 100487, 100488, 100490, 100491)

  5. 30.

    Ochotona pusilla (Pallas, 1769)—isolated teeth, late Pleistocene, Ranis, Germany (KOE 1415)

  6. 31.

    Ochotona pusilla (Pallas, 1769)—isolated teeth, late Pleistocene, Southern Germany (KOE 84, KOE 2832, and KOE 4071)

  7. 32.

    Ochotona sp.—five crania with mandibles, recent, Nepal (ZMFK 84.729, 84.730, 84.732, 84.733, 84.735)

  8. 33.

    Piezodus branssatensis (Viret, 1929)—several mandibles and maxillae, latest Oligocene MP 30, Coderet-Branssat, France, (NMB–Bst 227, 9409b, 9414, 3899 [CT scan resolution = 0.02264 mm, p4 m1 virtual resolution = 0.01134 mm], 9411, Cod 366, 3368, 369, 372, 373 [CT scan resolution = 0.0147 mm], 375, 378, 382, 383, 385, 403 and, 273)

  9. 34.

    Piezodus tomerdingensis Tobien, 1975—left maxilla with P2-M1, early Miocene, Tommerdingen, SW Germany, (SMNS 26001)

  10. 35.

    Prolagus oeningensis König, 1825—several isolated teeth, Miocene MN 7–8, La Grive M, France (KOE 1410–1411 [M sup, m inf, CT scans each with resolution = 0.00788 mm]

  11. 36.

    Prolagus sardus (Wagner, 1832)—several upper and lower jaws, Pleistocene, Mte. S. Giovanni near Carbonia, Sardinia (ded. Danilo Torre, KOE 1441) [upper jaw, CT scan resolution = 0.01597 mm]

  12. 37.

    Titanomys visenoviensis (von Meyer, 1843)—left mandible with and left maxilla with P4-M2, early Miocene MN1, Tommerdingen, SW Germany (SMNS 26048)

Characters in lagomorph cheek teeth

Dentiton

  1. 1.

    Hypsodonty: 0 = brachydont, 1= hypsodont and rooted, 2 = partial hypsodonty, 3 = euhypsodont.

  2. 2.

    p3 shape: 0 = ochotonid, 1 = palaeolagine, 2 = archaeolagine, 3= leporine.

  3. 3.

    Last upper molar: 0 = unreduced, 1= M3 small, 2 = M3 missing, 3 = M3 missing, extrafold on M2.

  4. 4.

    Last lower molar: 1 = m3 persent but reduced, 2= m3 missing, 3 = m2 with extrafold.

  5. 5.

    Connection between anterolophid and posterolophid: 0 = attached lingually, 1 = separated in youth, than attached lingually, 2 = medially attached by cementum.

  6. 6.

    irregular enamel in molars: 0 = HSB still recognizable, 1 = present.

Upper cheek teeth

  1. 7.

    Enamel thickness: 0 = undifferentiated, 1 = slight, 2 = well differentiated.

  2. 8.

    PSB, length and lingual side: 0 = absent, 1 = full length, 2 = partial, 3 = open for phase II’.

  3. 9.

    PSB striation: 0 = not visible, 1 = vertical, 2 = diagonal.

  4. 10.

    Lingual REF, length: 0 = shallow, 1 = half width, 2 = deep.

  5. 11.

    Lingual REF, enamel thickness: 0 = no inner part, 1 = equal, 2 = anterior side thickened, 3 = posterior side thickened.

  6. 12.

    Lingual REF, enamel crenulation: 0 = no crenulation, 1 = both sides equal, 2 = anterior side dominant, 3 = posterior side dominant.

  7. 13.

    SSB on posteroloph: 0 = absent, 1= composed, 2 = on posterior side (ochotonid).

  8. 14.

    SSB, striation: 0 = not visible, 1 = vertical, 2 = diagonal.

  9. 15.

    lagicone structure o P4-M2: 0 = lagicone structure in P3-M2, 1 = M1 without, P4 with lagicone, 2 = P4 to M2 without lagicone structure, 3 = p3 to M2 without lagicone structure.

  10. 16.

    SSB, length and lingual side: 0 = absent, 1 = full length, 2 = partial, 3 = open for phase I.

  11. 17.

    Enamel at protocone and hypocone: 0 = undifferentiated, pointed, 1 = thickened and facet flattened, 2 = obliquely flattened.

  12. 18.

    Posteroloph, posterior side: 0 = low, 1 = rising, part of PSB of following tooth.

  13. 19.

    TDF: 0 = absent, 1 = weak, 2 = rounded towards Ib-facet, 3 = well separated.

  14. 20.

    Dentine ridge in buccal prolongation of REF: 0 = absent, 1 = present.

  15. 21.

    REF as grinding surface or facet: 0 = no distinctive feature, 1 = grinding, 2 = shearing facet on anterior side (SSB), 3 = shearing blade on posterior side (SSB).

  16. 22.

    Facet for II’ phase: 0 = absent, 1 = present.

Lower cheek teeth.

  1. 23.

    Enamel thickness: 0 = undifferentiated, 1 = slight, 2 = well differentiated.

  2. 24.

    PSB on anterolophid: 0 = absent, 1 = present.

  3. 25.

    PSB, striation: 0 = not visible, 1 = vertical, 2 = diagonal.

  4. 26.

    Anterior side of anterolophid: 0 = high, 1 = sloping anteriorly, 2= slight crest of enamel band, 3 = part of SSB of the anterior tooth.

  5. 27.

    Buccal REF, crenulated enamel: 0 = absent, 1= crenulated on posterior side.

  6. 28.

    Anterior enamel band of posterolophid: 0 = not incorporated in PSB, 1= incorporated in PSB, 2 = partially incorporated and anterobuccally excavated.

  7. 29.

    Posterolophid, posterior side: 0 = thin or lingually thinning, 1 = thickened without facet, 2 = thickened with facet (SSB), 3 = additional fold (in Amphilagus and Titanomys), when young

  8. 30.

    SSB, Striation: 0 = not visible, 1 = vertical, 2 = diagonal.

  9. 31.

    Metaconid, striation: 0 = absent, 1 = facet, 2 = vertical striation.

  10. 32.

    Enamel at protoconid and hypoconid: 0 = undifferentiated, pointed, 1 = thickened and facet flattened, 2= obliquely flattened.

  11. 33.

    Facet for phase II’: 0 = absent, 1 = present.

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Koenigswald, W.v., Anders, U., Engels, S. et al. Tooth Morphology in Fossil and Extant Lagomorpha (Mammalia) Reflects Different Mastication Patterns. J Mammal Evol 17, 275–299 (2010). https://doi.org/10.1007/s10914-010-9140-z

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