The University of Southampton
University of Southampton Institutional Repository

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

The consequences of daily cyclic hypoxia on a European grass shrimp: from short-term responses to long-term effects
The consequences of daily cyclic hypoxia on a European grass shrimp: from short-term responses to long-term effects
1.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, characterized by profound variations in oxygen partial pressure (pO2) from supersaturated conditions (~42kPa) to extremely hypoxic conditions (~3kPa) in ~12‐hours.2.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 hours day−1 below 4.0kPa). In the laboratory adults were kept at water pO2 <4.5kPa for 7‐hours each night and in normoxic conditions for the rest of the time.3.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 μm2/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.4.On the first experimental day, in cyclic hypoxic exposed animals, we recorded a 50% decrease in feeding rates (during hypoxic conditions) in comparison to 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.
0269-8463
2333-2344
Peruzza, Luca
c01f028c-1fb4-44a4-83b9-f24698a9c9e5
Gerdol, Marco
06665026-fd50-4cb6-b310-ede42435ab4f
Oliphant, Andrew
a080aa80-9deb-4e70-aadb-7c0b02600735
Wilcockson, David
ba84a5a7-c06c-4d54-ba4d-1113c607e28e
Pallavicini, Alberto
250ed385-c46f-4011-92d8-34cb0039a627
Hawkins, Lawrence
9c4d1845-82db-4305-acb5-31b218ac9c0e
Thatje, Sven
f1011fe3-1048-40c0-97c1-e93b796e6533
Hauton, Chris
7706f6ba-4497-42b2-8c6d-00df81676331
Peruzza, Luca
c01f028c-1fb4-44a4-83b9-f24698a9c9e5
Gerdol, Marco
06665026-fd50-4cb6-b310-ede42435ab4f
Oliphant, Andrew
a080aa80-9deb-4e70-aadb-7c0b02600735
Wilcockson, David
ba84a5a7-c06c-4d54-ba4d-1113c607e28e
Pallavicini, Alberto
250ed385-c46f-4011-92d8-34cb0039a627
Hawkins, Lawrence
9c4d1845-82db-4305-acb5-31b218ac9c0e
Thatje, Sven
f1011fe3-1048-40c0-97c1-e93b796e6533
Hauton, Chris
7706f6ba-4497-42b2-8c6d-00df81676331

Peruzza, Luca, Gerdol, Marco, Oliphant, Andrew, Wilcockson, David, Pallavicini, Alberto, Hawkins, Lawrence, Thatje, Sven and Hauton, Chris (2018) The consequences of daily cyclic hypoxia on a European grass shrimp: from short-term responses to long-term effects. Functional Ecology, 32 (10), 2333-2344. (doi:10.1111/1365-2435.13150).

Record type: Article

Abstract

1.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, characterized by profound variations in oxygen partial pressure (pO2) from supersaturated conditions (~42kPa) to extremely hypoxic conditions (~3kPa) in ~12‐hours.2.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 hours day−1 below 4.0kPa). In the laboratory adults were kept at water pO2 <4.5kPa for 7‐hours each night and in normoxic conditions for the rest of the time.3.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 μm2/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.4.On the first experimental day, in cyclic hypoxic exposed animals, we recorded a 50% decrease in feeding rates (during hypoxic conditions) in comparison to 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.

Text
Peruzza_et_al-2018-Functional_Ecology (1) - Accepted Manuscript
Download (939kB)
Text
Peruzza_et_al-2018-Functional_Ecology Accepted manuscript
Restricted to Repository staff only
Request a copy

More information

Accepted/In Press date: 23 May 2018
e-pub ahead of print date: 1 June 2018

Identifiers

Local EPrints ID: 421622
URI: https://eprints.soton.ac.uk/id/eprint/421622
ISSN: 0269-8463
PURE UUID: 2e5269cd-462d-4a05-86e9-f15c00cc1822
ORCID for Lawrence Hawkins: ORCID iD orcid.org/0000-0002-9236-2396
ORCID for Chris Hauton: ORCID iD orcid.org/0000-0002-2313-4226

Catalogue record

Date deposited: 18 Jun 2018 16:30
Last modified: 14 Mar 2019 05:05

Export record

Altmetrics

Contributors

Author: Luca Peruzza
Author: Marco Gerdol
Author: Andrew Oliphant
Author: David Wilcockson
Author: Alberto Pallavicini
Author: Sven Thatje
Author: Chris Hauton ORCID iD

University divisions

Download statistics

Downloads from ePrints over the past year. Other digital versions may also be available to download e.g. from the publisher's website.

View more statistics

Atom RSS 1.0 RSS 2.0

Contact ePrints Soton: eprints@soton.ac.uk

ePrints Soton supports OAI 2.0 with a base URL of https://eprints.soton.ac.uk/cgi/oai2

This repository has been built using EPrints software, developed at the University of Southampton, but available to everyone to use.

We use cookies to ensure that we give you the best experience on our website. If you continue without changing your settings, we will assume that you are happy to receive cookies on the University of Southampton website.

×