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

Abstract

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.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Anderson, G. E., & Secor, S. M. (2015). Ontogenetic shifts and spatial associations in organ position for snakes. Zoology, 118(6), 403–418.

    Article  Google Scholar 

  2. Andrews, R. M. (1979). The lizard Corytophanes cristatus: an extreme “sit-and-wait” predator. Biotropica, 11(2), 136–139.

    Article  Google Scholar 

  3. Barden, A. (1943). Food of the basilisk lizard in Panama. Copeia, 1943(2), 118–121.

    Article  Google 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.

    Article  Google Scholar 

  7. Boback, S. M. (2005). Natural history and conservation of island boas (Boa constrictor) in Belize. Copeia, 2005, 880–885.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Google 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.

    Article  Google 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.

    Article  Google Scholar 

  16. Etheridge, R. (1967). Lizard caudal vertebrae. Copeia, 1967(4), 699–721.

    Article  Google Scholar 

  17. Fleet, R. R., & Fitch, A. J. (1974). Food habits of Basiliscus basiliscus in Costa Rica. Journal of Herpetology, 8(3), 260–262.

    Article  Google 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.

  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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google Scholar 

  26. Hallinan, T. (1920). Notes on lizards of the canal zone, Isthmus of Panama. Copeia, 83, 45–49.

    Article  Google 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.

    Article  Google 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.

    Article  Google Scholar 

  30. Henderson, R. W. (1993). Foraging and diet in West Indian Corallus enydris (Serpentes: Boidae). Journal of Herpetology, 27(1), 24–28.

    Article  Google 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.

    Article  Google 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.

    Article  Google Scholar 

  33. Hirth, H. F. (1963). The ecology of two lizards on a tropical beach. Ecological Monographs, 33(2), 83–112.

    Article  Google Scholar 

  34. Koenigswald, W. von, & Schaarschmidt, F. (1983). Ein Urpferd aus Messel, das Weinbeeren fraß. Natur und Museum, 113(3), 79–84.

  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.

    Article  Google 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.

  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.

  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.

    Article  Google 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.

    Article  Google Scholar 

  45. McCoy, C. J. (1968). A review of the genus Laemanctus (Reptilia, Iguanidae). Copeia, 1968(4), 665–678.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google Scholar 

  52. Retzius, A. (1830 [1831]) Anatomisk undersökning öfver nagra delar af Python bivittatus jemte comparative anmärkningar. Kongliga Vetenskapsacademiens Handlingar, 1830(1), 81–116.

  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.

    Article  Google 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.

    Article  Google 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.

    Article  Google Scholar 

  57. Sasa, M., & Monrós, J. S. (2000). Dietary analysis of helmeted basilisks, Corytophanes (Reptilia: Corytophanidae). Southwestern Naturalist, 45(3), 358–361.

    Article  Google 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.

  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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

  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.

    Article  Google 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 

Download references

Acknowledgements

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.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Krister T. Smith.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Smith, K.T., Scanferla, A. Fossil snake preserving three trophic levels and evidence for an ontogenetic dietary shift. Palaeobio Palaeoenv 96, 589–599 (2016). https://doi.org/10.1007/s12549-016-0244-1

Download citation

Keywords

  • Messel
  • Middle Eocene
  • Palaeopython fischeri
  • Geiseltaliellus maarius
  • Gut contents
  • Food chain