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Discontinuous ammonia excretion and glutamine storage in littoral Oniscidea (Crustacea: Isopoda): testing tidal and circadian models

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Abstract

A key evolutionary development facilitating land colonization in terrestrial isopods (Isopoda: Oniscidea) is the intermittent liberation of waste nitrogen as volatile ammonia. Intermittent ammonia release exploits glutamine (Gln) as an intermediary nitrogen store. Here, we explore the relationship between temporal patterns of ammonia release and Gln accumulation in three littoral oniscideans from Southern California. Results are interpreted in terms of water availability, habitat, activity patterns, and ancestry. A two-way experimental design was used to test whether ammonia excretion and Gln accumulation follow a tidal or diel periodicity. Ammonia excretion was studied in the laboratory using chambers with or without available seawater and using an acid trap to collect volatile ammonia. Ligia occidentalis releases ammonia directly into seawater and accumulates Gln during low tide (48.9 ± 6.5 μmol g−1 at low tide, 24.1 ± 3.0 μmol g−1 at high tide), indicating that excretion is tidally constrained. Alloniscus perconvexus and Tylos punctatus can excrete ammonia directly into seawater or utilize volatilization. Both species burrow in sand by day and show a diel excretory pattern, accumulating Gln nocturnally (31.8 ± 2.7 μmol g−1 at dawn and 21.8 ± 2.3 μmol g−1 at dusk for A. perconvexus; 85.7 ± 15.1 μmol g−1 at dawn and 25.4 ± 2.9 μmol g−1 at dusk for T. punctatus) and liberating ammonia diurnally. Glutaminase shows higher activity in terrestrial (0.54–0.86 U g−1) compared to intertidal (0.25–0.31 U g−1) species, consistent with the need to generate high PNH3 for volatilization. The predominant isoform in Armadillidium vulgare is phosphate dependent and maleate independent; phosphate is a plausible regulator in vivo.

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Acknowledgments

We thank Rebecca Abbey and Ken Hsin whose primary studies provided the impetus for this study, and Pomona College for support. Collection of animals was authorized by a Scientific Collecting Permit issued by the California Department of Fish and Game. The experiments comply with the National Institute of Health ‘“Principles of Animal Care”, Publication No. 86-23, 1985, and with current laws of the USA.

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  1. Department of Biology, Pomona College, 175 West 6th Street, Claremont, CA, 91711, USA

    Maya Nakamura & Jonathan C. Wright

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  1. Maya Nakamura
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  2. Jonathan C. Wright
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Correspondence to Jonathan C. Wright.

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Communicated by G. Heldmaier.

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Nakamura, M., Wright, J.C. Discontinuous ammonia excretion and glutamine storage in littoral Oniscidea (Crustacea: Isopoda): testing tidal and circadian models. J Comp Physiol B 183, 51–59 (2013). https://doi.org/10.1007/s00360-012-0694-3

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  • DOI: https://doi.org/10.1007/s00360-012-0694-3

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