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Effects of emersion on acid–base regulation, osmoregulation, and nitrogen physiology in the semi-terrestrial mangrove crab, Helice formosensis

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Abstract

Emersion limits water availability and impairs the gill function of water-breathing animals resulting in a reduced capacity to regulate respiratory gas exchange, acid–base balance, and nitrogenous waste excretion. Semi-terrestrial crustaceans such as Helice formosensis mitigate these physiological consequences by modifying and recycling urine and branchial water shifting some branchial workload to the antennal glands. To investigate how this process occurs, Helice formosensis were emersed for up to 160 h and their hemolymph and urinary acid–base, nitrogenous waste, free amino acids, and osmoregulatory parameters were investigated. Upon emersion, crabs experienced a respiratory acidosis that is restored by bicarbonate accumulation and ammonia reduction within the hemolymph and urine after 24 h. Prolonged emersion caused an overcompensatory metabolic alkalosis potentially limiting the crab’s ability to remain emersed. During the alkalosis, hemolymph ammonia was maintained at control levels while urinary ammonia remained reduced by 60% of control values. During emersion, ammonia may be temporarily converted to alanine as part of the Cahill cycle until re-immersion where crabs can revert alanine to ammonia for excretion coinciding with the crabs’ observed delayed ammonia excretion response. The presence of high hemolymph alanine concentrations even when immersed may indicate this cycle’s use outside of emersion or in preparation for emersion. Furthermore, H. formosensis appears to be uniquely capable of actively suppressing its rate of desiccation in absence of behavioral changes, in part by creating hyperosmotic urine that mitigates evaporative water loss.

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Acknowledgements

We would like to thank Nick Chaung for help locating and obtaining the crabs used in this study as well as E-Hong Instruments (Taipei, Taiwan) for allowing us to use their atomic absorption spectrophotometer throughout these experiments.

Funding

G.J.P.A. was funded by a National Science and Engineering Research Council (NSERC) CGS-D and the University of Manitoba’s Field Work Support Program, D.W. was funded by an NSERC Discovery grant (RGPIN/5013‐2018).

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  1. Department of Biological Sciences, University of Manitoba, Winnipeg, MB, Canada

    Garett Joseph Patrick Allen & Dirk Weihrauch

  2. Marine Research Station, Institute of Cellular and Organismal Biology, Academia Sinica, Yilan County, Taiwan ROC

    Min-Chen Wang & Yung-Che Tseng

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  1. Garett Joseph Patrick Allen
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GJPA designed the study, performed experiments, and wrote the manuscript. M-CW performed some cation measurements and amino acid measurements. Y-CT and DW helped design the experiment, revise the manuscript, and funded the research.

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Correspondence to Dirk Weihrauch.

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SI Figure 1.

Hemolymph (N = 6–12) and urinary (N = 4-12) essential amino acid composition of immersed (0-h) and emersed crabs over a 160-hour time-course exposure. Where data in not available for urinary concentrations no detectable amino acid presence was found. Values are represented as the mean ± S.E.M. (JPG 43 KB)

SI Figure 2.

Hemolymph (N = 6–12) non-essential amino acid composition of immersed (0-h) and emersed crabs over a 160-hour time-course exposure. Where data in not available for urinary concentrations no detectable amino acid presence was found. Values are represented as the mean ± S.E.M. (JPG 80 KB)

SI Figure 3.

Urinary (N = 4–12) non-essential amino acid composition of immersed (0-h) and emersed crabs over a 160-hour time-course exposure. Where data in not available for urinary concentrations no detectable amino acid presence was found. Values are represented as the mean ± S.E.M. (JPG 64 KB)

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Allen, G.J.P., Wang, MC., Tseng, YC. et al. Effects of emersion on acid–base regulation, osmoregulation, and nitrogen physiology in the semi-terrestrial mangrove crab, Helice formosensis. J Comp Physiol B 191, 455–468 (2021). https://doi.org/10.1007/s00360-021-01354-0

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