Incisor Enamel Microstructure of Hystricognathous and Anomaluroid Rodents from the Earliest Oligocene of Dakhla, Atlantic Sahara (Morocco)

  • Laurent Marivaux
  • Myriam Boivin
  • Sylvain Adnet
  • Mohamed Benammi
  • Rodolphe Tabuce
  • Mouloud Benammi
Original Paper


Seven hystricognaths and five anomaluroids have been recently described from the earliest Oligocene of the Dakhla (DAK C2) region of Morocco, based primarily on isolated cheek teeth. Here, we analyzed the enamel microstructure of thirty associated isolated fragments of incisors. Among these specimens, only three display an early stage of uniserial Hunter-Schreger bands (HSBs), with mostly a single prism per band, but also occasionally two prisms per band (in two specimens), and a thin interprismatic matrix (IPM) that runs parallel to the prism direction, thereby documenting incisors of anomaluroids. All other sampled incisors display an enamel with multiserial HSBs, thereby documenting hystricognaths. For these latter, we recorded primarily an IPM crystallite arrangement describing the subtype 2 of multiserial HSBs, but with variation including a wide amplitude in the angle (acute) formed between the crystallites of IPM and those of the prisms, some variations in the frequency of the IPM sheet anastomoses, in the number of prisms per HSBs, and variations in the inclination of the HSBs. The absence of the subtypes 2–3 and 3 of multiserial HSBs in DAK C2 suggests that African hystricognathous rodents had still not achieved these most resistant multiserial HSBs at that time. The drier, cooler climatic regime of the early Oligocene, having increased the fragmentation and opening of habitats, might have played a role in the subsequent selection of taxa having acquired a more resistant incisor enamel.


Africa Paleogene Rodentia Uniserial Multiserial 



We are indebted to Henri Cappetta (ISE-M), Sébastien Enault (ISE-M), Jérôme Surault (iPHEP), Imad Elkati, Abdallah Tarmidi, Mbarek Fouadasi, and the local people of Dakhla for their assistance during the successive field seasons (2009-2017). We are grateful to Sandra Unal (ISE-M), Suzanne Jiquel (ISE-M), Bernard Marandat (ISE-M), Théo Mancuso (Université de Montpellier), and Jérôme Surault (iPHEP) for their contribution in the picking of the fossil specimens from Porto Rico (Pto) and El Argoub (Arg). We warmly thank Thomas Martin (Universität Bonn, Germany) for his useful advice regarding the enamel microstructure of rodent incisors. Many thanks to Chantal Cazevieille and Alicia Caballero-Megido (Montpellier RIO Imaging [MRI] and Institute for Neurosciences Montpellier [INM], France) for access to scanning electron microscope (SEM) facilities. We also thank the two anonymous external reviewers, who provided formal reviews of this manuscript that enhanced the final version. This research was supported by the French ANR-ERC PALASIAFRICA (ANR-08-JCJC-0017) and ANR EVAH (ANR-09-BLAN-0238) programs, the MEDYNA program (Maghreb-Eu research staff exchange on geoDYnamics, geohazards and applied geology in Northwest Africa; FP7, PIRSES-GA-2013-612572), and by the ISE-M UMR CNRS/UM/IRD/EPHE 5554 (Laboratoire de Paléontologie) and iPHEP UMR CNRS 7262. This is ISE-M publication 2018-001 SUD.

Supplementary material

10914_2017_9426_MOESM1_ESM.xlsx (14 kb)
ESM 1 Incisor enamel microstructure for extant and extinct Ctenohystrica. The bibliographic references are those of the main text. (XLSX 13 kb)
10914_2017_9426_MOESM2_ESM.xlsx (11 kb)
ESM 2 Incisor enamel microstructure for extant and extinct Anomaluroidea. The bibliographic references are those of the main text. (XLSX 10 kb)


  1. Adnet S, Cappetta H, Enault S, Benammi M, Marivaux L, Tabuce R, Saddiqi O, Baidder L, Benammi M (2017) The late Eocene/Oligocene elasmobranch fauna of the Samlat Formation in Dakhla, Morocco: a mirror of the coeval World Heritage sites of Egypt. The First West African Craton and Margins International Workshop (WACMA1), Dakhla. Abstract Volume: 81-82Google Scholar
  2. Benammi M, Adnet S, Marivaux L, Yans J, Noiret C, Tabuce R, Surault J, El Kati I, Enault S, Baidder L, Saddiqi O, Benammi M (2017) Geology, biostratigraphy and carbon isotope chemostratigraphy of the Paleogene fossil-bearing Dakhla sections, southwestern Moroccan Sahara. Geol Mag in press.
  3. Berggren WA, Prothero DR (1992) Eocene-Oligocene Climatic and Biotic Evolution: An Overview. Princeton University Press, PrincetonCrossRefGoogle Scholar
  4. Boivin M, Marivaux L, Salas-Gismondi R, Vieytes EC, Antoine P-O (2018) Incisor enamel microstructure of Paleogene caviomorph rodents from Contamana and Shapaja (Peruvian Amazonia). J Mammal Evol.
  5. Coiffait PE, Coiffait B, Jaeger J-J, Mahboubi M (1984) Un nouveau gisement à mammifères fossiles d'âge Éocène supérieur sur le versant Sud des Nementcha (Algérie orientale) : découverte des plus anciens rongeurs d'Afrique. C R Acad Sc Paris 13:893-898Google Scholar
  6. Coster P, Benammi M, Lazzari V, Billet G, Martin T, Salem M, Bilal AA, Chaimanee Y, Schuster M, Valentin X, Brunet M, Jaeger J-J (2010) Gaudeamus lavocati sp. nov. (Rodentia, Hystricognathi) from the early Oligocene of Zallah, Libya: first African caviomorph? Naturwissenschaften 97(8):697-706CrossRefPubMedGoogle Scholar
  7. Coster P, Benammi M, Salem M, Bilal AA, Chaimanee Y, Valentin X, Brunet M, Jaeger J-J (2012) New hystricognath rodents from the lower Oligocene of central Libya (Zallah Oasis, Sahara desert): systematic, phylogeny and biochronologic implications. Ann Carnegie Mus 80:239-259Google Scholar
  8. Coster PMC, Beard KC, Salem MJ, Chaimanee Y, Jaeger J-J (2015) New fossils from the Paleogene of central Libya illuminate the evolutionary history of endemic African anomaluroid rodents. Frontiers Earth Sci 3(56):1-15Google Scholar
  9. Coxall HK, Wilson P, Palike H, Lear C, Backman J (2005) Rapid stepwise onset of Antarctic glaciation and deeper calcite compensation in the Pacific Ocean. Nature 433:53-57CrossRefPubMedGoogle Scholar
  10. Dawson MR, Marivaux L, Li C-K, Beard KC, Métais G (2006) Laonastes and the "lazarus effect" in Recent mammals. Science 311:1456-1458CrossRefPubMedGoogle Scholar
  11. Holroyd PA (1994) An examination of dispersal origins for Fayum mammals. PhD Dissertation, Duke University, DurhamGoogle Scholar
  12. Hren MT, Sheldon ND, Grimes ST, Collinson ME, Hooker JJ, Bugler M, Lohmann KC (2013) Terrestrial cooling in Northern Europe during the Eocene-Oligocene transition. Proc Natl Acad Sci USA 110:7562-7567CrossRefPubMedPubMedCentralGoogle Scholar
  13. Jaeger J-J, Marivaux L, Salem M, Bilal AA, Chaimanee Y, Marandat B, Valentin X, Duringer P, Schuster M, Benammi M, Métais E, Brunet M (2010) New rodent assemblages from the Eocene Dur at-Talah escarpment (Sahara of central Libya): systematic, biochronologic and paleobiogeographic implications. Zool J Linn Soc 160:195-213CrossRefGoogle Scholar
  14. Koenigswald W von, Sander PM (1997) Glossary of terms used for enamel microstructures. In: Koenigswald W von, Sander PM (eds) Tooth Enamel Microstructure. Balkema, Rotterdam, pp 267-280Google Scholar
  15. Korvenkontio VA (1934) Mikroskopische Untersuchungen an Nagerincisiven unter Hinweis auf die Schmelzstruktur der Backenzähne. Ann Zoo Soc Zool – Bota Fennicae Vanamo 2:1-274Google Scholar
  16. Lear CH, Bailey TR, Pearson PN, Coxall HK, Rosenthal Y (2008) Cooling and ice growth across the Eocene-Oligocene transition. Geology 36:251-254CrossRefGoogle Scholar
  17. Marivaux L (2000) Les rongeurs de l'Oligocène des Collines Bugti (Balouchistan, Pakistan): nouvelles données sur la phylogénie des rongeurs paléogènes, implications biochronologiques et paléobiogéographiques. PhD Dissertation, Université Montpellier II, Sciences et Techniques du LanguedocGoogle Scholar
  18. Marivaux L, Adaci M, Bensalah M, Gomes Rodrigues H, Hautier L, Mahboubi M, Mebrouk F, Tabuce R, Vianey-Liaud M (2011) Zegdoumyidae (Rodentia, Mammalia), stem anomaluroid rodents from the early to middle Eocene of Algeria (Gour Lazib, western Sahara): new dental evidence. J Syst Palaeontol 9(4):563-588CrossRefGoogle Scholar
  19. Marivaux L, Adnet S, Benammi M, Tabuce R, Benammi M (2017a) Anomaluroid rodents from the earliest Oligocene of Dakhla, Morocco, reveal the long-lived and morphologically conservative pattern of the Anomaluridae and Nonanomaluridae during the Tertiary in Africa. J Syst Palaeontol 15(7):539-569CrossRefGoogle Scholar
  20. Marivaux L, Adnet S, Benammi M, Tabuce R, Yans J, Benammi M (2017b) Earliest Oligocene hystricognathous rodents from the Atlantic margin of northwestern Saharan Africa (Dakhla, Morocco): systematic, paleobiogeographical and paleoenvironmental implications. J Vertebr Paleontol 37(5):e1357567; CrossRefGoogle Scholar
  21. Marivaux L, Benammi M, Ducrocq S, Jaeger J-J, Chaimanee Y (2000) A new baluchimyine rodent from the late Eocene of the Krabi Basin (Thailand): paleobiogeographic and biochronologic implications. C R Acad Sc Paris 331(6):427-433Google Scholar
  22. Marivaux L, Chaimanee Y, Yamee C, Srisuk P, Jaeger J-J (2004) Discovery of Fallomus ladakhensis Nanda & Sahni, 1998 (Rodentia, Diatomyidae) in the lignites of Nong Ya Plong (Phetchaburi Province, Thailand): systematic, biochronologic and paleoenvironmental implications. Geodiversitas 26(3):493-507Google Scholar
  23. Marivaux L, Ducrocq S, Jaeger J-J, Marandat B, Sudre J, Chaimanee Y, Tun ST, Htoon W, Soe AN (2005) New remains of Pondaungimys anomaluropsis (Rodentia, Anomaluroidea) from the latest middle Eocene Pondaung Formation of central Myanmar. J Vertebr Paleontol 25(1):214-227CrossRefGoogle Scholar
  24. Marivaux L, Essid EM, Marzougui W, Khayati Ammar H, Adnet S, Marandat B, Merzeraud G, Tabuce R, Vianey-Liaud M (2014) A new and primitive species of Protophiomys (Rodentia, Hystricognathi) from the late middle Eocene of Djebel el Kébar, central Tunisia. Palaeovertebrata 38(1-e2):1–17Google Scholar
  25. Marivaux L, Essid EM, Marzougui W, Khayati Ammar H, Merzeraud G, Tabuce R, Vianey-Liaud M (2015) The early evolutionary history of anomaluroid rodents in Africa: new dental remains of a zegdoumyid (Zegdoumyidae, Anomaluroidea) from the Eocene of Tunisia. Zool Scripta 44(2):117-134CrossRefGoogle Scholar
  26. Marivaux L, Lihoreau F, Manthi KF, Ducrocq R (2012) A new basal phiomorph (Rodentia, Hystricognathi) from the late Oligocene of Lokone (Turkana Basin, Kenya). J Vertebr Paleontol 32(3):646-657CrossRefGoogle Scholar
  27. Martin T (1992) Schmelzmikrostruktur in den Inzisiven alt und neuweltlicher hystricognather Nagetiere. Palaeovertebrata Mém extra: 1-168Google Scholar
  28. Martin T (1993) Early rodent incisor enamel evolution: phylogenetic implications. J Mammal Evol 1(4):227-254CrossRefGoogle Scholar
  29. Martin T (1994) African origin of caviomorph rodents is indicated by incisor enamel microstructure. Paleobiology 20(1):5-13CrossRefGoogle Scholar
  30. Martin T (1995) Incisor enamel microstructure and phylogenetic interrelationships of Pedetidae and Ctenodactyloidea (Rodentia). Berliner Geowiss Abh 16:693-707Google Scholar
  31. Martin T (1997) Incisor enamel microstructure and systematics in rodents. In: Koenigswald W von, Sander PM (eds) Tooth Enamel Microstructure. Balkema, Rotterdam, pp 163-175Google Scholar
  32. Martin T (2004) Incisor enamel microstructure of South America's earliest rodents: implications for caviomorph origin and diversification. In: Campbell KE (ed) The Paleogene Mammalian Fauna of Santa Rosa, Amazonian Peru. Nat Hist Mus Los Angeles County, Los Angeles, pp 131-140Google Scholar
  33. Martin T (2005) Incisor schmelzmuster diversity in South America's oldest rodent fauna and early caviomorph history. J Mammal Evol 12(3/4):405-417CrossRefGoogle Scholar
  34. Martin T (2007) Incisor enamel microstructure and the concept of Sciuravida. In: Beard KC, Luo Z-X (eds) Mammalian Paleontology on a Global Stage: Papers in Honor of Mary R. Dawson. Bull Carnegie Mus Nat Hist 39:127-140CrossRefGoogle Scholar
  35. Morgan CC, Verzi DH, Olivares AI, Vieytes EC (2017) Craniodental and forelimb specializations for digging in the South American subterranean rodent Ctenomys (Hystricomorpha, Ctenomyidae). Mammal Biol 87:118-124CrossRefGoogle Scholar
  36. Noiret C, Benammi M, Adnet S, Enault S, Marivaux L, Tabuce R, Surault J, Baidder L, Saddiqi O, El Kati I, Benammi M, Yans J (2017) Carbon isotope chemostratigraphy on organics (δ13Corg): a powerful tool to refine the Paleogene age of the fossil-bearing levels in the Dakhla area (southwestern Moroccan Sahara). The First West African Craton and Margins International Workshop (WACMA1), Dakhla. Abstract Volume: 79-80.Google Scholar
  37. Sallam HM, Seiffert ER (2016) New phiomorph rodents from the latest Eocene of Egypt, and the impact of Bayesian “clock”-based phylogenetic methods on estimates of basal hystricognath relationships and biochronology. PeerJ 4(e1717)1-53Google Scholar
  38. Sallam HM, Seiffert ER, Simons EL (2010a) A highly derived anomalurid rodent from the earliest late Eocene of Egypt. Palaeontology 53(4):803-813CrossRefGoogle Scholar
  39. Sallam HM, Seiffert ER, Simons EL (2011) Craniodental morphology and systematics of a new family of hystricognathous rodents (Gaudeamuridae) from the late Eocene and early Oligocene of Egypt. PLoS One 6(2):1-29CrossRefGoogle Scholar
  40. Sallam HM, Seiffert ER, Simons EL (2012) A basal phiomorph (Rodentia, Hystricognathi) from the late Eocene of the Fayum Depression, Egypt. Swiss J Palaeontol 131(2):283-301CrossRefGoogle Scholar
  41. Sallam HM, Seiffert ER, Simons EL, Brindley C (2010b) A large-bodied anomaluroid rodent from the earliest late Eocene of Egypt: phylogenetic and biogeographic implications. J Vertebr Paleontol 30(5):1579-1593CrossRefGoogle Scholar
  42. Sallam HM, Seiffert ER, Steiper ME, Simons EL (2009) Fossil and molecular evidence constrain scenarios for the early evolutionary and biogeographic history of hystricognathous rodents. Proc Natl Acad Sci USA 106:16722-16727CrossRefPubMedPubMedCentralGoogle Scholar
  43. Thomas H, Roger J, Sen S, Al-Sulaimani Z (1992) Early Oligocene vertebrates from Dhofar (Sultanate of Oman). In: Sadek A (ed) Geology of the Arab World. Cairo University, Cairo, pp 283-293Google Scholar
  44. Thomas H, Roger S, Sen S, Bourdillon-de-Grissac C, Al-Sulaimani Z (1989) Découverte de vertébrés fossiles dans l'Oligocène inférieur du Dhofar (Sultanat d'Oman). Geobios 22(1):101-120CrossRefGoogle Scholar
  45. Tramoy R, Salpin M, Schnyder J, Person A, Sebilo M, Yans J, Vaury V, Fozzani J, Bauer H (2016) Stepwise palaeoclimate change across the Eocene–Oligocene transition recorded in continental NW Europe by mineralogical assemblages and δ15Norg (Rennes Basin, France). Terra Nova 28(3):212-220CrossRefGoogle Scholar
  46. Vieytes EC (2003) Microestructura del esmalte de roedores Hystricognathi sudamericanos fósiles y vivientes: significado morfofuncional y filogenético. PhD Dissertation, Universidad Nacional de La Plata, La PlataGoogle Scholar
  47. Vieytes EC, Morgan CC, Verzi DH (2007) Adaptive diversity of incisor enamel microstructure in South American burrowing rodents (family Ctenomyidae, Caviomorpha). J Anat 211(3):296-302CrossRefPubMedPubMedCentralGoogle Scholar
  48. Vucetich MG, Vieytes EC (2006) A middle Miocene primitive octodontoid rodent and its bearing on the early evolutionary history of the Octodontoidea. Palaeontographica Abt A 277:81–91Google Scholar
  49. Vucetich MG, Vieytes EC, Pérez ME, Carlini AA (2010) The rodents from La Cantera and the early evolution of caviomorphs in South America. In: Madden RH, Carlini AA, Vucetich MG, Kay RF (eds) The Paleontology of Gran Barranca, Evolution and Environmental Change through the Middle Cenozoic of Patagonia. Cambridge University Press, Cambridge, pp 189–201Google Scholar
  50. Wood AE (1968) Part II: The African Oligocene Rodentia. In: Remington JE (Ed) Early Cenozoic Mammalian Faunas Fayum Province, Egypt. Peabody Mus Nat Hist Yale Univ, New Haven, pp 23-105Google Scholar
  51. Zachos JC, Dickens GR, Zeebe RE (2008) An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics. Nature 451: 279–283CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Laboratoire de Paléontologie, Institut des Sciences de l’Évolution de Montpellier (ISE-M, UMR 5554, CNRS/UM/IRD/EPHE)Université de MontpellierMontpellierFrance
  2. 2.Laboratoire de Géologie Géophysique Géorisques et Environnement (3GE), Faculté des SciencesUniversité Ibn TofailKénitraMorocco
  3. 3.Institut de Paléoprimatologie, Paléontologie Humaine: Évolution et Paléoenvironnements (iPHEP, UMR-CNRS 7262), UFR SFAUniversité de PoitiersPoitiersFrance

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