Abstract
Inflammatory arthritis is documented for the first time in snakes. Ossification of the intervertebral capsule and zygapophyseal joints resulting in segmental vertebral fusion was observed in the aquatic Cretaceous snake Lunaophis aquaticus. Such pathologic alterations are pathognomonic for the spondyloarthropathy form of inflammatory arthritis. A survey of 2144 snakes in recent collections, performed to identify Holocene prevalence, revealed only two occurrences in extant snakes. The findings in Bitis gabonica and Elaphe taeniura were indistinguishable from those noted in Lunaophis aquaticus and identical to those previously recognized in modern varanids. The pathology likely represents a form of reactive arthritis related to enteropathic infection. While the disease probably did not affect general locomotion, its vertebral column position may have compromised mating.
This is a preview of subscription content, log in via an institution to check access.
References
Albino AM, Carrillo-Briceño JD, Neenan JM (2016) An enigmatic aquatic snake from the Cenomanian of Northern South America. Peer J 4:e2027. https://doi.org/10.7717/peerj.2027
Altman RD, Singer F (1980) Paget’s disease of bone. Proceedings of the Kroc Foundation Conference (March 24-March 28, Santa Ynez Valley, California). Arthritis Rheum 23:1073–1234
Brownstein DG, Stgrandbert JD, Montali RJ, Bush M, Foretner J (1977) Cryptosporidium in snakes with hypertrophic gastritis. Vet Pathol 14:606–617
Burnham DA, Rothschild BM, Babiarz J, Martin LD (2013) Hemivertebrae as pathology and as a window to behavior in the fossil record. PalArch’s J Vert Palaeontol 10:1–6
Feldtkeller E, Rothschild B (in press) Spondyloarthritis in antiquity and history. In: Inman R, Sieper J (eds) Oxford textbook of axial spondyloarthritis. Oxford University Press, Oxford. https://doi.org/10.1093/med/9780198734444.003.0001
Frye FL, Carney J (1974) Osteitis deformans (Paget’s disease) in a boa constrictor. Vet Med Small Anim Clin 69:186–188
Guinot G, Carrillo-Briceño J (2018) Lamniform sharks from the Cenomanian (upper Cretaceous) of Venezuela. Cretac Res 82:1–20. https://doi.org/10.1016/j.cretres.2017.09.021
Houssaye A (2009) “Pachyostosis” in aquatic amniotes: a review. Integrative Zool 4:325–340
Houssaye A (2010) Rediscovery and description of the second specimen of the hindlimbed snake Pachyophis woodwardi Nopcsa 1923 (Squamata, Ophidia) from the Cenomanian of Bosnia Herzegovina. J Vert Paleontol 30:276–279. https://doi.org/10.1080/02724630903416043
Hsiang AY, Field DJ, Webster TH, Behlke ADB, Davis MB, Racicot RA, Gauthier JA (2015) The origin of snakes: revealing the ecology, behavior, and evolutionary history of early snakes using genomics, phenomics, and the fossil record. BMC Evol Biol 5:–87. https://doi.org/10.1186/s12862-015-0358-5
Isaza R, Garner M, Jacobson E (2000) Proliferative osteoarthritis and osteoarthrosis in 15 snakes. J Zoo Wildl Med 31:20–27
Jacobson ER (2007) Infectious diseases and pathology of reptiles: color atlas and text. CRC Press, Boca Raton
Lee MSY, Caldwell MW (1998) Anatomy and relationships of Pachyrhachis problematicus, a primitive snake with hindlimbs. Phil Trans R Soc Lond B 353:1521–1552. https://doi.org/10.1098/rstb.1998.0308
Marcus LC (1981) Veterinary biology and medicine of captive amphibians and reptiles. Lea and Febiger, Philadelphia
Nime FA, Burek JD, Page DL, Holscher MA, Yaardley JH (1976) Acute enterocolitis in a human being infected with the protozoan Cryptosporidium. Gastroenterology 70:592–598
Rage JC, Vullo R, Néraudeau D (2016) The mid-Cretaceous snake Simoliophis rochebrunei (Sauvage, 1880) (Squamata: Ophidia) from its type area (Charentes, southwestern France): redescription, distribution, and palaeoecology. Cretac Res 58:234–253. https://doi.org/10.1016/j.cretres.2015.10.010
Resnick D (2002) Diagnosis of bone and joint disorders. Saunders, Philadelphia
Rothschild BM (2009) Scientifically rigorous reptile and amphibian osseous pathology: lessons for forensic herpetology from comparative and paleo-pathology. Appl Herpetol 6:47–79. https://doi.org/10.1163/157075409X413842
Rothschild BM, Everhart MJ (2015) Co-ossification of vertebrae in mosasaurs (Squamata, Mosasauridae); evidence of habitat interactions and susceptibility to bone disease. Trans Kans Acad Sci 118:265–275. https://doi.org/10.1660/062.118.0309
Rothschild BM, Martin LD(2006) Skeletal impact of disease. New Mexico Museum of Natural History Press, Alburquerque.fv
Rothschild BM, Schultze HP, Pellegrini R (2012) Herpetological osteopathology: annotated bibliography of amphibians and reptiles. Springer, New York
Acknowledgments
Appreciation is expressed to David Dickey, David Kiziriain, Steve Rogers, Kenneth Tighe, and Loren Vonahme for hosting access to the collections they curate, and to members of the Evolutionary Morphology and Palaeobiology group at the University of Zurich for generous collaboration.
Funding
This paper was supported by Consejo Nacional de Investigaciones Científicas y Técnicas grant to A.M.A (CONICET-PIP 112-201501-00065), Swiss National Science Foundation grant (31003A-149605, awarded to Marcelo Sánchez-Villagra), and Leverhulme Trust Early Career Fellowship (ECF-2017-360, awarded to J.M.N).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by: Sven Thatje
Rights and permissions
About this article
Cite this article
Albino, A.M., Rothschild, B., Carrillo-Briceño, J.D. et al. Spondyloarthropathy in vertebrae of the aquatic Cretaceous snake Lunaophis aquaticus, and its first recognition in modern snakes. Sci Nat 105, 51 (2018). https://doi.org/10.1007/s00114-018-1576-7
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00114-018-1576-7