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

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 (pO2) 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 pO2 < 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 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. 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 http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13150/suppinfo is available for this article.

Oxygen‐mediated plasticity confers hypoxia tolerance in a corallivorous polychaete

“…These types of responses have primarily been observed in species inhabiting chronic hypoxia and are thought to be evolutionary adaptations to relatively stable low DO conditions (Levin, ). Complementary studies on intermittent hypoxia have documented similar modifications, such as increased gill growth in European grass shrimp from salt marsh habitats with severe daily oxygen fluctuations (Peruzza et al, ). These few studies additionally suggest that traits developing after short bouts of severe intermittent hypoxia can be quite different to those found in chronic hypoxia exposures and may have more to do with the species' recovery period rather than persistence through hypoxic periods (Borowiec, Darcy, Gillette, & Scott, ; Peruzza et al, ).…”

“…These types of responses have primarily been observed in species inhabiting chronic hypoxia and are thought to be evolutionary adaptations to relatively stable low DO conditions (Levin, 2003). Complementary studies on intermittent hypoxia have documented similar modifications, such as increased gill growth in European grass shrimp from salt marsh habitats with severe daily oxygen fluctuations (Peruzza et al, 2018).…”

“…These few studies additionally suggest that traits developing after short bouts of severe intermittent hypoxia can be quite different to those found in chronic hypoxia exposures and may have more to do with the species' recovery period rather than persistence through hypoxic periods (Borowiec, Darcy, Gillette, & Scott, 2015;Peruzza et al, 2018).…”

Vulnerability of juvenile hermit crabs to reduced seawater pH and shading

“…Within coastal ecosystems, crustaceans provide several ecological and economic services (LeBlanc, 2007) playing an important role in the structure of food webs (Laidre and Greggor, 2015;Shaffer et al, 1995) and energy flux (Kristensen, 2008;Robertson, 1986). Therefore, the impacts of environmental stressors on crustaceans have been well studied (e.g., hypoxia, Peruzza et al, 2018;hypercapnia, Borges et al, 2018;salinity fluctuations, Joseph and Philip, 2007;and pollutants, Vogt et al, 2018) and sublethal effects are known to cause physiological disruption (LeBlanc, 2007;Moullac and Haffner, 2000), which thereby induce impairments in behavioral performance (Felten et al, 2008;Hebel et al, 1997;Tuomainen and Candolin, 2010).…”

Respiratory Metabolism Responses of Chinese Mitten Crab, Eriocheir sinensis and Chinese Grass Shrimp, Palaemonetes sinensis, Subjected to Environmental Hypoxia Stress

“…For example, environmental hypoxia causes abnormal breathing and metabolic disorders in crustaceans, which leads to a decline in feeding and efficiency of food transformation and retarded growth ( Han et al, 2017 ; Sun et al, 2018 ). Environmental hypoxia even affects the behavior, morphological characteristics, immunity, and reproduction of crustaceans ( De Lima et al, 2015 ; Lara et al, 2017 ; Peruzza et al, 2018 .).…”