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Wide scope for ammonia and urea excretion in foraging Pacific hagfish

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Abstract

Hagfish (Myxinidae) are jawless, marine vertebrates that feed on decaying carrion drops on the ocean floor. Although food consumption rates have not been measured, it is likely that hagfish ingest large amounts of protein during such feeding bouts. Thus, they would be expected to have a high scope for amino acid catabolism which would result in high rates of post-feeding ammonia and urea excretion. Hagfish could also be exposed to high amounts of ammonia as they burrow into the decomposing carcasses during feeding. The goal of the present study was to determine if foraging Pacific hagfish (Eptatretus stoutii) have a higher capacity than other fish species to unload the large amounts of ammonia and urea which may accumulate in their body after feeding. Accordingly, ammonia (J Amm) and urea-N (J Urea) excretion rates were measured immediately following the removal of Pacific hagfish from cylindrical Korean cone-traps, which had been baited with decomposing hake and submerged in the Trevor Channel, off Bamfield, British Columbia. The rate of J Amm in the foraging hagfish averaged 674 ± 210 µmol N kg−1 h−1 over the first 1 h following removal from the traps, which was 21-fold greater than measurements made in non-fed control hagfish. By 4–6 h, J Amm was 50% lower than the 1 h post-foraging rate, before stabilizing between 48–72 h. Post-foraging J Urea was ninefold greater than in the unfed control hagfish, averaging 116 ± 21 µmol N kg−1 h−1 during the first 2 h. Over the next 24–48 h, J Urea gradually declined, before approaching rates measured in the unfed hagfish. Despite high post-foraging J Amm, plasma total ammonia (T Amm) concentrations were surprisingly low, averaging 114–226 µmol N L−1, but still 4.5 to 9-fold higher than in their unfed counterparts. Plasma urea-N concentrations were higher, averaging 1838 ± 376 µmol N L−1 in the unfed fish, but were unchanged following foraging. The very high factorial scope (21-fold) for J Amm compared to other fishes, suggests that hagfish have a high capacity to excrete ammonia arising from amino acid catabolism, as well as ammonia that may be incidentally taken-up as a result of their feeding behaviour. The relatively high urea excretion capacity of hagfish, may be important for rapidly off-loading urea which arises from the hydrolysis of dietary arginine due to the ingestion of decomposing tissue from dead fishes, or after urea is ingested from decomposing elasmobranchs or marine mammals.

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Acknowledgements

We wish to thank Janice Pierce and the rest of the staff at the Bamfield Marine Science Centre (BMSC) for their invaluable assistance with the capture of Pacific hagfish, and their hospitality. We are also grateful to Dr. Chris Wood for helpful discussions concerning the design and interpretation of our experiments. Margo Couse provided invaluable technical assistance with the processing and analysis of blood and tissues at Wilfrid Laurier University, and was funded by a Natural Sciences and Engineering Research Council of Canada (NSERC) Undergraduate Student Research Award.

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Correspondence to Michael P. Wilkie.

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This study was funded by Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grants to MPW (04248) and GGG (203736). AMC was supported by an NSERC—PGSD (370386), The Alberta Innovates Technology Futures—Omics Scholarship, The President’s Doctoral Prize of Distinction, The Donald M. Ross Memorial Scholarship, The R. E. (Dick) Peter Memorial Scholarship, The Andrew Stewart Memorial Prize, The Western Canadian Universities Marine Sciences Society Graduate Student Award and the Dick and Leona Peter BMSC residential bursary. Each of MPW, SLE, AMC or GGG declare that they have no conflict of interests. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed as described in the “Materials and methods”.

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Wilkie, M.P., Clifford, A.M., Edwards, S.L. et al. Wide scope for ammonia and urea excretion in foraging Pacific hagfish. Mar Biol 164, 126 (2017). https://doi.org/10.1007/s00227-017-3148-3

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