Deep vs. Shallow Diving Marine Mammals: Variation in Complement Responses and Susceptibility to Dive-Related Injury
Activation of inflammatory responses via the complement cascade has been linked to damage associated with decompression sickness (DCS) in humans. In 2017, our lab presented data indicating that the complement response to nitrogen bubbles, measured as changes in C5a, in belugas (Delphinapterus leucas) and harbor seals (Phoca vitulina) is less sensitive than in humans (Homo sapiens), but that circulating C5a may vary based on physiology (e.g. stress). Results of that work also suggested differences in sensitivity threshold between the two species, with free ranging belugas displaying an increase in C5a following the high flow rate of N2 (i.e. smaller bubbles, but more bubbles) while harbor seals displayed increased C5a in response to the lowest flow rate (fewer, larger bubbles). While belugas are capable of diving deeper than 1000 m, the belugas used in this study have limited dive environments whether under professional care in an aquarium, or from a coastal population. Similarly harbor seals usually dive to only a few hundred meters. This project aimed to investigate whether a deep diving cetacean and phocid display similar responses, and if dive ability may be a predictor of sensitivity to DCS-like injury. Serum samples were obtained from 5 narwhal (Monodon monoceros) and 10 Weddell seals (Leptonychotes weddellii) including 5 adults and 5 pups, during either live capture health assessment efforts or during collaborative research efforts in Antarctica, respectively. Serum was exposed to nitrogen bubbles for a duration of 30 minutes at two flow rates, 0.5 and 1 ml min-1, which have been shown to result in complement activation in humans and rabbits. The complement component 5a (C5a) was measured with and without nitrogen exposures as a marker of activation of inflammatory responses. Control measures of C5a were not significantly different in narwhal as compared with belugas, nor between adult and pup Weddell seals. However Weddell seals did have significantly higher control C5a as compared with release (i.e. healthy) harbor seals even when only age matched animals were compared (Kruskal Wallis; p=0.004; adults p=0.042, pups p=0.019). No significant change in C5a was detected for narwhal following either nitrogen exposure, and this was significantly different than the previously measured significant increase in C5a in Bristol Bay belugas following exposure to 1 ml min-1 (p=0.017). No significant effect of nitrogen exposures was detected for the Weddell seals, and no significant difference in response was detected between Weddell seals and harbor seals. This project continues our unique research investigating the relationship between diving and health in marine mammals, lending further support to the hypothesis of a less reactive immune response serving a protective function in diving mammals. That the live capture sampled narwhal and live capture sampled belugas responded differently to the highest flow suggests that beluga may be more at risk of dive related injury particularly under stressor conditions, or for example, if their natural dive patterns are altered.
The authors would like to especially thank Dr. Sandra Black for providing narwhal serum samples and Dr. Allyson Hindle for providing Weddell seal serum (NMFS permit #19439 and ACA permit #2016-005, NSF Award #1443554). Samples were received under the National Marine Fisheries Service Permit #17298. Previous beluga and harbor seal work was supported by the Office of Naval Research award #N000141512203.