Miceala M. Shocklee1*+; Alexandra R. Emelianchik1; Margo A. Lillie2; David S. Rotstein3; Robert J. Ossiboff1; Michael T. Walsh1
Abstract
Between 2012 and 2020, four deceased dolphins from three Stenella spp. (frontalis, longirostris, coeruleoalba) recovered from stranding cases were presented to the University of Florida for post-mortem. Prior to necropsy, computed tomography (CT) was performed. In three cases, a one- to two-part, curvilinear, U- to J-shaped osseous structure was found within the diaphragmatic musculature at the rostral aspect of the aortic hiatus. The osseous structure, herein referred to as the os diaphragm, was found in an adult female Stenella longirostris, an adult male and gravid adult female Stenella frontalis. A developing, non-ossified, cartilaginous os diaphragm was also found in the late second-trimester fetus of the gravid S. frontalis. No os diaphragm was found in an adult, gravid Stenella coeruleoalba or in the fetus. Partial to nearly whole diaphragm sections with the in situ osseous structure were removed for further imaging. The section of S. longirostris diaphragm with bone in situ and a section of the S. frontalis fetus diaphragm were also examined histologically.
As determined via the “virtopsy” approach combining CT imaging of the intact specimens with traditional pathology techniques, the os diaphragm appears to be a normal finding in some Stenella spp. and is consistent with a true bone serving a functional anatomic role. This distinction sets the Stenella os diaphragm apart from structures like the os cordis described in other species.1–5 Previous research into the only other reported os diaphragm, found in Camelus dromedarius, as well as prior reports on cetacean diaphragm functional anatomy, suggest that the Stenella os diaphragm may aid in resisting compression of the aortic hiatus under tension.5–7 Diving and hunting habits of S. frontalis and S. longirostris in comparison to those of S. coeruleoalba do not immediately suggest why the former species would require an os diaphragm and not the latter. The small sample size and the prior finding in camels that some individuals within the population lacked the os diaphragm prompt further investigation in Stenella spp.8–10 This case series also provides further encouragement to pair pre-necropsy imaging modalities with 3D rendering capability with more traditional necropsy approaches to expand the exploratory and diagnostic power of post-mortem examinations.14
Acknowledgments
The authors would like to thank the Emerald Coast Wildlife Refuge, Nadia Gordon and the Florida Fish and Wildlife Conservation Commission, and Abby Stone and all of the Clearwater Marine Aquarium team for their aid in recovering these animals. The authors would like to thank the University of Florida radiology service, especially Mary Wilson, Bobbie Davis, Dr. David Reese, Dr. Aitor Gallastegui, and Dr. Elodie Huguet for their immense assistance with imaging these animals. The authors also extend our gratitude to Mary Duncan and the St. Louis Zoo for sharing their experience with the camel os diaphragm.
Literature Cited
1. Ghonimi W, Balah A, Bareedy MH, Abuel-Atta AA. 2014. Os cordis of The Mature Dromedary Camel Heart (Camelus dromedaries) with Special Emphasis to The Cartilago Cordis. Veterinary Science & Technology 5(4):1.
2. Frink RJ, Merrick B. 1974. The sheep heart: coronary and conduction system anatomy with special reference to the presence of an os cordis. The Anatomical Record, 179(2):189–199.
3. Egerbacher M, Weber H, Hauer S. 2000. Bones in the heart skeleton of the otter (Lutra lutra). The Journal of Anatomy 196(3): 485–491.
4. Etemadi AA. 1966. Diaphragm and os diaphragmaticum in Camelus dromedarius. Cells Tissues Organs 65(4): 551–560.
5. Taher ES, El-Gaafary MA, Al-Shaikhly AK. 1975. Some studies of the centrum tendineum of the diaphragm of camel (Camelus dromedarius). Anatomischer Anzeiger 138(3):192–202.
6. Cotten PB, Piscitelli MA, McLellan WA, Rommel SA, Dearolf JL, Pabst DA. 2008. The gross morphology and histochemistry of respiratory muscles in bottlenose dolphins, Tursiops truncatus. Journal of Morphology 269(12): 1520–1538.
7. Lillie MA, Vogl AW, Raverty S, Haulena M, McLellan WA, Stenson GB, Shadwick RE. 2017. Controlling thoracic pressures in cetaceans during a breath-hold dive: importance of the diaphragm. Journal of Experimental Biology 220(19): 3464–3477.
8. Scott MD, Chivers SJ. 2009. Movements and diving behavior of pelagic spotted dolphins. Marine Mammal Science, 25(1): 137–160.
9. Davis RW, Worthy GA, Würsig B, Lynn SK, Townsend FI. 1996. Diving behavior and at‐sea movements of an Atlantic spotted dolphin in the Gulf of Mexico. Marine Mammal Science 12(4): 569–581.
10. Bolliger SA, Thali MJ, Ross S, Buck U, Naether S, Vock P. 2008. Virtual autopsy using imaging: bridging radiologic and forensic sciences. A review of the Virtopsy and similar projects. European radiology 18(2): 273–282.