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Variation in the hemostatic complement (C5a) responses to in vitro nitrogen bubbles in monodontids and phocids

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Abstract

Immune responses to nitrogen gas bubbles, particularly activation of inflammation via the complement cascade, have been linked to the development of symptoms and damage associated with decompression sickness (DCS) in humans. Marine mammals were long thought not to be susceptible to such dive-related injury, yet evidence of DCS-like injury and new models of tissue nitrogen super-saturation suggest that bubbles may routinely form. As such, it is possible that marine mammals have protective adaptations that allow them to deal with a certain level of bubble formation during normal dives, without acute adverse effects. This work evaluated the complement response, indicative of inflammation, to in vitro nitrogen bubble exposures in several marine mammal species to assess whether a less-responsive immune system serves a protective role against DCS-like injury in these animals. Serum samples from beluga (Delphinapterus leucas), and harbor seals (Phoca vitulina) (relatively shallow divers) and deep diving narwhal (Monodon monoceros), and Weddell seals (Leptonychotes weddellii) were exposed to nitrogen bubbles in vitro. Complement activity was evaluated by measuring changes in the terminal protein C5a in serum, and results suggest marine mammal complement is less sensitive to gas bubbles than human complement, but the response varies between species. Species-specific differences may be related to dive ability, and suggest moderate or shallow divers may be more susceptible to DCS-like injury. This information is an important consideration in assessing the impact of changing dive behaviors in response to anthropogenic stressors, startle responses, or changing environmental conditions that affect prey depth distributions.

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Acknowledgements

Funding for this work was provided by the Office of Naval Research Award Number N000141512203. The authors would like to thank the Animal Care department at Mystic Aquarium for sample collection, as well as the Beluga Husbandry and Marine Mammal Rescue and Rehabilitation staff. Thank you to the veterinary and animal care staff at Sea World San Antonio and Sea World Orlando for contributing beluga serum samples to this project. Fieldwork in Bristol Bay was made possible by Dr. Caroline Goertz and Dr. Roderick Hobbs, as well as the Bristol Bay Native Association, Bristol Bay Marine Mammal Council, the Alaska Beluga Committee and the Alaska Department of Fish and Game. Field efforts in Bristol Bay, AK were funded by the Georgia Aquarium. This research was conducted under Mystic Aquarium IACUC #15004. Wild beluga sampling efforts were conducted under NMFS permit 14245. Collection of Weddell seal samples was supported by NSF # 1443554/1921491 and authorized by NMFS #19439, #1,662 and ACA #2016-005. Narwhal and Weddell seal serum were received under NMFS Permit #17298. This constitutes scientific publication #305 from Sea Research Foundation, Inc.

Funding

This works was funded by the Office of Naval Research Award Number N000141512203.

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LT conceived of the study, carried out analyses and wrote the manuscript; AH and SB contributed new resources for the research, without which the manuscript would not exist in its current form, and contributed to manuscript editing; TR contributed to interpretation of data analyses and manuscript writing.

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Correspondence to Laura A. Thompson.

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This research was conducted under Mystic Aquarium IACUC #15004. Wild beluga sampling efforts were conducted under NMFS permit 14245. Collection of Weddell seal samples was supported by NSF # 1443554/1921491 and authorized by NMFS #19439, #18662 and ACA #2016-005. Narwhal and Weddell seal serum were received under NMFS Permit #17298.

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Communicated by H.V. Carey.

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Thompson, L.A., Hindle, A.G., Black, S.R. et al. Variation in the hemostatic complement (C5a) responses to in vitro nitrogen bubbles in monodontids and phocids. J Comp Physiol B 190, 811–822 (2020). https://doi.org/10.1007/s00360-020-01297-y

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