Palaeobiodiversity and Palaeoenvironments

, Volume 96, Issue 4, pp 589–599 | Cite as

Fossil snake preserving three trophic levels and evidence for an ontogenetic dietary shift

  • Krister T. SmithEmail author
  • Agustín Scanferla
Original Paper


We report a fossil snake from the middle Eocene (48 Ma) Messel Pit, in whose stomach is a lizard, in whose stomach is an insect. This is the second known vertebrate fossil containing direct evidence of three trophic levels. The snake is identified as a juvenile of Palaeopython fischeri on the basis of new characters of the skull; the lizard is identified as Geiseltaliellus maarius, a stem-basilisk; and the insect, despite preserved structural colouration, could not be identified more precisely. G. maarius is thought to have been an arboreal species, but like its extant relatives may have foraged occasionally on the ground. Another, larger specimen of G. maarius preserves plant remains in the digestive tract, suggesting that omnivory in this species may have been common in larger individuals, as in extant Basiliscus and Polychrus. A general picture of the trophic ecology of P. fischeri is not yet possible, although the presence of a lizard in the stomach of a juvenile individual suggests that this snake could have undergone a dietary shift, as in many extant boines.


Messel Middle Eocene Palaeopython fischeri Geiseltaliellus maarius Gut contents Food chain 



The specimen was prepared by Bruno Behr (SMF) and photographed by Anika Vogel (SMF). Peter Hornberger (Technische Hochschule Deggendorf) conducted the CT scans of SMF ME 11332, and Wieland Binczik and Heike Scherf (University of Tübingen) of SMF ME 11398. Gotthard Richter (SMF) helped with the SEMs. Juliane Eberhart (SMF) inked the drawings of the snake. Anika Vogel (SMF) assembled the drawings and other figures. Volker Wilde and Dieter Uhl (SMF) helped with the interpretation of the plant remains, and Sonja Wedmann (SMF) with the insect. We are grateful to them all, and to Stephan Schaal (SMF) for discussion. Finally, we thank Jean-Claude Rage (Muséum National d’Histoire Naturelle, Paris) and Annelise Folie (Royal Belgian Institute of Natural Sciences, Brussels) for their helpful reviews, which improved this paper.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Anderson, G. E., & Secor, S. M. (2015). Ontogenetic shifts and spatial associations in organ position for snakes. Zoology, 118(6), 403–418.CrossRefGoogle Scholar
  2. Andrews, R. M. (1979). The lizard Corytophanes cristatus: an extreme “sit-and-wait” predator. Biotropica, 11(2), 136–139.CrossRefGoogle Scholar
  3. Barden, A. (1943). Food of the basilisk lizard in Panama. Copeia, 1943(2), 118–121.CrossRefGoogle Scholar
  4. Baszio, S. (2004). Messelophis variatus n. gen. n. sp. from the Eocene of Messel: a tropidopheine snake with affinities to Erycinae (Boidae). Courier Forschungsinstitut Senckenberg, 252, 47–66.Google Scholar
  5. Blain, A. W., & Campbell, K. N. (1942). A study of digestive phenomena in snakes with the aid of Roentgen ray. American Journal of Roentgenology and Radium Therapy, 48, 229–239.Google Scholar
  6. Blob, R. W. (1998). Evaluation of vent position from lizard skeletons for estimation of snout–vent length and body mass. Copeia, 1998(3), 792–801.CrossRefGoogle Scholar
  7. Boback, S. M. (2005). Natural history and conservation of island boas (Boa constrictor) in Belize. Copeia, 2005, 880–885.CrossRefGoogle Scholar
  8. Buchy, M.-C., & Smith, K. T. (2011). New portions of the holotype of Vallecillosaurus donrobertoi (Squamata, Mosasauroidea) from the early Turonian (Upper Cretaceous) of Mexico. In J. Calvo, J. Porfiri, B. González Riga, & D. Dos Santos (Eds.), Paleontología y dinosaurios desde América Latina. Mendoza, Argentina: Editorial de la Universidad Nacional de Cuyo.Google Scholar
  9. Conrad, J. L. (2015). A new Eocene casquehead lizard (Reptilia, Corytophanidae) from North America. PLoS One, 10(7), e0127900.CrossRefGoogle Scholar
  10. Cooper, W. E., Jr., & Vitt, L. J. (2002). Distribution, extent, and evolution of plant consumption by lizards. Journal of Zoology, London, 257, 487–517.CrossRefGoogle Scholar
  11. Cundall, D., & Greene, H. W. (2000). Feeding in snakes. In K. Schwenk (Ed.), Feeding: form, function and evolution in tetrapod vertebrates (pp. 293–333). San Diego: Academic Press.CrossRefGoogle Scholar
  12. de Avila Pires, T. C. S. (1995). Lizards of Brazilian Amazonia (Reptilia: Squamata). Zoologische Verhandellingen, 299, 1–706.Google Scholar
  13. de Queiroz, A., & de Queiroz, K. (1987). Prey handling behavior of Eumeces gilberti with comments on headfirst ingestion in squamates. Journal of Herpetology, 21(1), 57–63.CrossRefGoogle Scholar
  14. Duellman, W. E. (1990). Herpetofaunas in neotropical rainforests: comparative composition, history, and resource use. In A. H. Gentry (Ed.), Four neotropical rainforests (pp. 455–505). New Haven, Connecticut: Yale University Press.Google Scholar
  15. Echelle, A. A., Echelle, A. F., & Fitch, H. S. (1972). Observations of fish-eating and maintenance behavior in two species of Basiliscus. Copeia, 1972(2), 387–389.CrossRefGoogle Scholar
  16. Etheridge, R. (1967). Lizard caudal vertebrae. Copeia, 1967(4), 699–721.CrossRefGoogle Scholar
  17. Fleet, R. R., & Fitch, A. J. (1974). Food habits of Basiliscus basiliscus in Costa Rica. Journal of Herpetology, 8(3), 260–262.CrossRefGoogle Scholar
  18. Franzen, J. L. (1997). Ein Koprolith als Leckerbissen. Der siebte Primatenfund aus Messel. Natur und Museum, 127(2), 46–53.Google Scholar
  19. Franzen, J. L. (2007). Eozäne Equoidea (Mammalia, Perissodactyla) aus der Grube Messel bei Darmstadt (Deutschland): Funde der Jahre 1969–2000. Schweizerische Paläontologische Abhandlungen, 127, 1–245.Google Scholar
  20. Gailer, J. P., Calandra, I., Schulz-Kornas, E., & Kaiser, T. M. (2016) Morphology is not destiny: discrepancy between form, function and dietary adaptation in bovid cheek teeth. Journal of Mammalian Evolution, In press.Google Scholar
  21. Garda, A. A., Costa, G. C., França, F. G. R., Giugliano, L. G., Leite, G. S., Mesquita, D. O., et al. (2012). Reproduction, body size, and diet of Polychrus acutirostris (Squamata: Polychrotidae) in two contrasting environments in Brazil. Journal of Herpetology, 46(1), 2–8.CrossRefGoogle Scholar
  22. Gauthier, J., Kearney, M., Maisano, J. A., Rieppel, O., & Behlke, A. (2012). Assembling the squamate tree of life: perspectives from the phenotype and the fossil record. Bulletin of the Peabody Museum of Natural History, 53, 3–308.CrossRefGoogle Scholar
  23. Goth, K. (1990). Der Messeler Ölschiefer - ein Algenlaminit. Courier Forschungsinstitut Senckenberg, 131, 1–141.Google Scholar
  24. Greene, H. W. (1983). Dietary correlates of the origin and radiation of snakes. American Zoologist, 23, 431–441.CrossRefGoogle Scholar
  25. Habersetzer, J., Richter, G., & Storch, G. (1994). Paleoecology of early middle Eocene bats from Messel, FRG: aspects of flight, feeding and echolocation. Historical Biology, 8(1–4), 235–260.CrossRefGoogle Scholar
  26. Hallinan, T. (1920). Notes on lizards of the canal zone, Isthmus of Panama. Copeia, 83, 45–49.CrossRefGoogle Scholar
  27. Harlow, P., & Shine, R. (1992). Food habits and reproductive biology of the Pacific Island Boas Candoia. Journal of Herpetology, 26(1), 60–66.CrossRefGoogle Scholar
  28. Harris, V. A. (1963). The anatomy of the rainbow lizard Agama agama (L) with a glossary of anatomical terms (Hutchinson tropical monographs). London: Hutchinson.Google Scholar
  29. Helmstetter, C., Pope, R. K., T’Flachebba, M., Secor, S. M., & Lignot, J.-H. (2009). The effects of feeding on the morphology and proliferation of the gastrointestinal tract of juvenile Burmese pythons (Python molurus). Canadian Journal of Zoology, 87, 1255–1267.CrossRefGoogle Scholar
  30. Henderson, R. W. (1993). Foraging and diet in West Indian Corallus enydris (Serpentes: Boidae). Journal of Herpetology, 27(1), 24–28.CrossRefGoogle Scholar
  31. Henderson, R. W., Noeske-Hallin, T. A., Ottenwalder, J. A., & Schwartz, A. (1987). On the diet of the boa Epicrates striatus on Hispaniola, with notes on Epicrates fordi and Epicrates gracilis. Amphibia-Reptilia, 8, 251–258.CrossRefGoogle Scholar
  32. Henderson, R. W., & Pauers, M. J. (2012). On the diets of Neotropical treeboas (Squamata: Boidae: Corallus). South American Journal of Herpetology, 7(2), 172–180.CrossRefGoogle Scholar
  33. Hirth, H. F. (1963). The ecology of two lizards on a tropical beach. Ecological Monographs, 33(2), 83–112.CrossRefGoogle Scholar
  34. Koenigswald, W. von, & Schaarschmidt, F. (1983). Ein Urpferd aus Messel, das Weinbeeren fraß. Natur und Museum, 113(3), 79–84.Google Scholar
  35. Köhler, G. (2008). Reptiles of Central America (2nd ed.). Herpeton Verlag: Offenbach am Main.Google Scholar
  36. Kriwet, J., Witzmann, F., Klug, S., & Heidtke, U. H. (2009). First direct evidence of a vertebrate three-level trophic chain in the fossil record. Proceedings of the Royal Society of London, Series B, 275, 181–186.CrossRefGoogle Scholar
  37. Lee, J. C. (1996). The amphibians and reptiles of the Yucatan Peninsula. Ithaca, New York: Cornell University Press.Google Scholar
  38. Lee, J. C. (2000). A Field guide to the amphibians and reptiles of the Maya world: the lowlands of Mexico, Northern Guatemala, and Belize. Ithaca, New York: Cornell University Press.Google Scholar
  39. Lenz, O., Wilde, V., Mertz, D. F., & Riegel, W. (2015). New palynology-based astronomical and revised 40Ar/39Ar ages for the Eocene maar lake of Messel (Germany). International Journal of Earth Sciences, 104, 873–889.Google Scholar
  40. Lindgren, J., Caldwell, M. W., Konishi, T., & Chiappe, L. M. (2010). Convergent evolution in aquatic tetrapods: insights from an exceptional fossil mosasaur. PLoS One, 5(8), e11998.Google Scholar
  41. Loop, M. S., & Bailey, L. G. (1972). The effect of relative prey size on the ingestion behavior of rodent-eating snakes. Psychonomic Science, 28(3), 167–169.CrossRefGoogle Scholar
  42. Losos, J. B. (2011). Lizards in an evolutionary tree. Berkeley, California: University of California Press.Google Scholar
  43. Martin, J. E., & Fox, J. E. (2007). Stomach contents of Globidens, a shell-crushing mosasaur (Squamata), from the Late Cretaceous Pierre Shale Group, Big Bend area of the Missouri River, central South Dakota. Geological Society of America Special Paper, 427, 167–176.Google Scholar
  44. Mayr, G., & Wilde, V. (2014). Eocene fossil is earliest evidence of flower-visiting by birds. Biology Letters, 10(5), 20140223.CrossRefGoogle Scholar
  45. McCoy, C. J. (1968). A review of the genus Laemanctus (Reptilia, Iguanidae). Copeia, 1968(4), 665–678.CrossRefGoogle Scholar
  46. McNamara, M. E., Briggs, D. E. G., Orr, P. J., Wedmann, S., Noh, H., & Cao, H. (2011). Fossilized biophotonic nanostructures reveal the original colors of 47-million-year-old moths. Plos Biology, 9(11), e1001200.CrossRefGoogle Scholar
  47. Mori, A. (1991). Effects of prey size and type on prey-handling behavior in Elaphe quadrivirgata. Journal of Herpetology, 25(2), 160–166.CrossRefGoogle Scholar
  48. Parker, A. R., & McKenzie, D. R. (2003). The cause of 50 million-year-old colour. Proceedings of the Royal Society of London, Series B, 270, S151–S153.CrossRefGoogle Scholar
  49. Pizzatto, L., Marques, O. A. V., & Facure, K. (2009). Food habits of Brazilian boid snakes: overview and new data, with special reference to Corallus hortulanus. Amphibia-Reptilia, 30(4), 533–544.CrossRefGoogle Scholar
  50. Pyron, R. A., Burbrink, F. T., & Wiens, J. J. (2013). A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evolutionary Biology, 13, 93.CrossRefGoogle Scholar
  51. Reeder, T. W., Townsend, T. M., Mulcahy, D. G., Noonan, B. P., Wood, P. L., Jr., Sites, J. W., et al. (2015). Integrated analyses resolve conflicts over squamate reptile phylogeny and reveal unexpected placements for fossil taxa. PLoS One, 10(3), e0118199.CrossRefGoogle Scholar
  52. Retzius, A. (1830 [1831]) Anatomisk undersökning öfver nagra delar af Python bivittatus jemte comparative anmärkningar. Kongliga Vetenskapsacademiens Handlingar, 1830(1), 81–116.Google Scholar
  53. Reynolds, A. E. (1939). Some gross anatomical relations of the male urogenital system and other internal organs in Eumeces fasciatus. Proceedings of the Indiana Academy of Science, 49, 233–242.Google Scholar
  54. Reynolds, R. G., Niemiller, M. L., & Revell, L. J. (2014). Toward a Tree-of-Life for the boas and pythons: multilocus species-level phylogeny with unprecedented taxon sampling. Molecular Phylogenetics and Evolution, 71, 201–213.CrossRefGoogle Scholar
  55. Richter, G., & Baszio, S. (2001). Traces of a limnic food web in the Eocene Lake Messel—a preliminary report based on fish coprolite analyses. Palaeogeography, Palaeoclimatology, Palaeoecology, 166(3), 345–368.CrossRefGoogle Scholar
  56. Richter, G., & Wedmann, S. (2005). Ecology of the Eocene Lake Messel revealed by analysis of small fish coprolites and sediments from a drilling core. Palaeogeography, Palaeoclimatology, Palaeoecology, 223(1), 147–161.CrossRefGoogle Scholar
  57. Sasa, M., & Monrós, J. S. (2000). Dietary analysis of helmeted basilisks, Corytophanes (Reptilia: Corytophanidae). Southwestern Naturalist, 45(3), 358–361.CrossRefGoogle Scholar
  58. Scanferla, C. A., Smith, K. T., & Schaal, S. F. K. (2016). Revision of the cranial anatomy and phylogenetic relationships of the Eocene minute boas Messelophis variatus and Messelophis ermannorum (Serpentes, Booidea). Zoological Journal of the Linnean Society, 176, 182–206.Google Scholar
  59. Schaal, S. (2004). Palaeopython fischeri n. sp. (Serpentes: Boidae), eine Riesenschlange aus dem Eozän (MP 11) von Messel. Courier Forschungsinstitut Senckenberg, 252, 35–45.Google Scholar
  60. Schaal, S., & Baszio, S. (2004). Messelophis ermannorum n. sp., eine neue Zwergboa (Serpentes: Boidae: Tropidopheinae) aus dem Mittel-Eozän von Messel. Courier Forschungsinstitut Senckenberg, 252, 67–77.Google Scholar
  61. Secor, S. M. (2008). Digestive physiology of the Burmese python: broad regulation of integrated performance. Journal of Experimental Biology, 211(24), 3767–3774.CrossRefGoogle Scholar
  62. Secor, S. M., & Diamond, J. M. (1995). Adaptive responses to feeding in Burmese pythons: pay before pumping. Journal of Experimental Biology, 198(6), 1313–1325.Google Scholar
  63. Secor, S. M., & Diamond, J. M. (2000). Evolution of regulatory responses to feeding in snakes. Physiological and Biochemical Zoology, 73(2), 123–141.CrossRefGoogle Scholar
  64. Sironi, M., Chiaraviglio, M., Cervantes, R., Bertona, M., & Rio, M. (2000). Dietary habits of Boa constrictor occidentalis, in the Cordoba Province, Argentina. Amphibia-Reptilia, 21, 226–232.Google Scholar
  65. Skoczylas, R. (1970). Influence of temperature on gastric digestion in the grass snake, Natrix natrix, L. Comparative Biochemistry and Physiology, 33, 793–804.CrossRefGoogle Scholar
  66. Slowinski, J. B., & Savage, J. M. (1995). Urotomy in Scaphiodontophis: evidence for the multiple tail break hypothesis in snakes. Herpetologica, 51(3), 338–341.Google Scholar
  67. Smith, K. T. (2009). Eocene lizards of the clade Geiseltaliellus from Messel and Geiseltal, Germany, and the early radiation of Iguanidae (Squamata: Iguania). Bulletin of the Peabody Museum of Natural History, 50(2), 219–306.CrossRefGoogle Scholar
  68. Smith, K. T., & Wuttke, M. (2012). From tree to shining sea: taphonomy of the arboreal lizard Geiseltaliellus maarius from Messel, Germany. In M. Wuttke, A.G. Reisdorf (Eds.) Taphonomic processes in terrestrial and marine environments. Palaeobiodiversity and Palaeoenvironments, 92(1), 45–65.Google Scholar
  69. Ungar, P. S. (2010). Mammal teeth: origin, evolution, and diversity. Baltimore, Maryland: Johns Hopkins University Press.Google Scholar
  70. Vitt, L. J., & Lacher, T. E., Jr. (1981). Behavior, habitat, diet, and reproduction of the iguanid lizard Polychrus acutirostris in the caatinga of northeastern Brazil. Herpetologica, 37(1), 53–63.Google Scholar
  71. Weber, S. (2004). Ornatocephalus metzleri gen. et spec. nov. (Lacertilia, Scincoidea)—taxonomy and paleobiology of a basal scincoid lizard from the Messel Formation (middle Eocene: basal Lutetian, Geiseltalium), Germany. Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft, 561, 1–159.Google Scholar
  72. Williams, E. (1972). The origin of faunas. Evolution of lizard congeners in a complex island fauna: a trial analysis. Evolutionary Biology, 6, 47–89.CrossRefGoogle Scholar
  73. Zaher, M., El-Ghareeb, A.-W., Hamdi, H., Essa, A., & Lahsik, S. (2012). Anatomical, histological and histochemical adaptations of the reptilian alimentary canal to their food habits: I. Uromastyx aegyptiaca [sic]. Life Science Journal, 9(3), 84–104.Google Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of Palaeoanthropology and Messel ResearchSenckenberg Research InstituteFrankfurt am MainGermany
  2. 2.CONICET-Instituto de Bio y Geociencias del NOA (IBIGEO)Rosario de LermaArgentina

Personalised recommendations