The consequences of daily cyclic hypoxia on a European grass shrimp: From short‐term responses to long‐term effects

Luca Peruzza, Marco Gerdol, Andrew Oliphant, David Wilcockson, Alberto Pallavicini, Lawrence Hawkins, Sven Thatje, Chris Hauton

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Abstract

Salt marshes are a key coastal environment for their important role as nursery habitats for marine and estuarine fish and crustaceans. Salt marshes are variable environments where species can experience daily cyclic hypoxic stress, characterised by profound variations in oxygen partial pressure (pO 2) from supersaturated conditions (~42 kPa) to extremely hypoxic conditions (~3 kPa) in ~12-hr. Here, under laboratory conditions, we assessed the physiological consequences of exposing the shrimp Palaemon varians, a species commonly found in the salt marshes of northern Europe, to the daily cyclic hypoxic regime currently experienced in its habitat in August (7.1 ± 1.8 hr/day below 4.0 kPa). In the laboratory, adults were kept at water pO 2 < 4.5 kPa for 7 hr each night and in normoxic conditions for the rest of the time. We recorded an acceleration of P. varians’ moult cycle, which was 15% shorter in animals kept in cyclic hypoxia compared to animals in normoxia. Similarly, the pattern of expression of two cuticular proteins over an entire moult cycle indicated an effect of cyclic hypoxia on moult stage-related genes. After 16 days, morphological changes to the gills were detected, with shrimps in cyclic hypoxia having a 13.6% larger lamellar surface area (measured in μm 2/mg animal) than normoxic animals, which could improve gas exchange capacity. Overall, phenotypic and morphological data indicate that faster moulting is triggered in response to cyclic hypoxia, with the benefit that gill modifications can be prompted more rapidly in order to meet oxygen requirements of the body. On the first experimental day, in cyclic hypoxic-exposed animals, we recorded a 50% decrease in feeding rates (during hypoxic conditions) in comparison with normoxic animals. Similarly, ammonium excretion was reduced by 66%–75% during the 1st and 21st experimental day. Body size was reduced by ~4% after 28 days. Females that reproduced in cyclic hypoxic conditions reduced the amount of yolk in each egg by ~24%. Overall, results underline how, in a decapod shrimp living in a key coastal environment, many physiological parameters are impaired by a cyclic hypoxic regime that is currently found in its natural habitat. A plain language summary is available for this article.

Original languageEnglish
Pages (from-to)2333-2344
Number of pages12
JournalFunctional Ecology
Volume32
Issue number10
Early online date19 Jun 2018
DOIs
Publication statusPublished - 04 Oct 2018

Keywords

  • cyclic hypoxia
  • shrimp
  • transcriptomics
  • gill morphology
  • moult cycle
  • body size
  • reproduction
  • ammonium excretion

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