Fish embryo vulnerability to combined acidification and warming coincides with a low capacity for homeostatic regulation

The vulnerability of fish embryos and larvae to environmental factors is often attributed to a lack of adult-like organ systems (gills) and thus insufficient homeostatic capacity. However, experimental data supporting this hypothesis are scarce. Here, by using Atlantic cod (Gadus morhua) as a model,...

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Published in:Journal of Experimental Biology
Main Authors: Dahlke, Flemming, Lucassen, Magnus, Bickmeyer, Ulf, Wohlrab, Sylke, Puvanendran, Velmurugu, Mortensen, Atle, Chierici, Melissa, Pörtner, Hans-Otto, Storch, Daniela
Format: Article in Journal/Newspaper
Language:unknown
Published: 2020
Subjects:
Online Access:https://epic.awi.de/id/eprint/52355/
https://doi.org/10.1242/jeb.212589
https://hdl.handle.net/10013/epic.5507d777-665c-4936-9acc-34573911bc38
id ftawi:oai:epic.awi.de:52355
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spelling ftawi:oai:epic.awi.de:52355 2024-09-15T17:55:34+00:00 Fish embryo vulnerability to combined acidification and warming coincides with a low capacity for homeostatic regulation Dahlke, Flemming Lucassen, Magnus Bickmeyer, Ulf Wohlrab, Sylke Puvanendran, Velmurugu Mortensen, Atle Chierici, Melissa Pörtner, Hans-Otto Storch, Daniela 2020 https://epic.awi.de/id/eprint/52355/ https://doi.org/10.1242/jeb.212589 https://hdl.handle.net/10013/epic.5507d777-665c-4936-9acc-34573911bc38 unknown Dahlke, F. , Lucassen, M. orcid:0000-0003-4276-4781 , Bickmeyer, U. orcid:0000-0002-5351-2902 , Wohlrab, S. orcid:0000-0003-3190-0880 , Puvanendran, V. , Mortensen, A. , Chierici, M. , Pörtner, H. O. orcid:0000-0001-6535-6575 and Storch, D. orcid:0000-0003-3090-7554 (2020) Fish embryo vulnerability to combined acidification and warming coincides with a low capacity for homeostatic regulation , The Journal of Experimental Biology, 223 (11), jeb212589 . doi:10.1242/jeb.212589 <https://doi.org/10.1242/jeb.212589> , hdl:10013/epic.5507d777-665c-4936-9acc-34573911bc38 EPIC3The Journal of Experimental Biology, 223(11), pp. jeb212589, ISSN: 0022-0949 Article isiRev 2020 ftawi https://doi.org/10.1242/jeb.212589 2024-06-24T04:24:41Z The vulnerability of fish embryos and larvae to environmental factors is often attributed to a lack of adult-like organ systems (gills) and thus insufficient homeostatic capacity. However, experimental data supporting this hypothesis are scarce. Here, by using Atlantic cod (Gadus morhua) as a model, the relationship between embryo vulnerability (to projected ocean acidification and warming) and homeostatic capacity was explored through parallel analyses of stage-specific mortality and in vitro activity and expression of major ion pumps (ATP-synthase, Na+/K+-ATPase, H+-ATPase) and co-transporters (NBC1, NKCC1). Immunolocalization of these transporters was used to study ionocyte morphology in newly hatched larvae. Treatment-related embryo mortality until hatching (+20% due to acidification and warming) occurred primarily during an early period (gastrulation) characterized by extremely low ion transport capacity. Thereafter, embryo mortality decreased in parallel with an exponential increase in activity and expression of all investigated ion transporters. Significant changes in transporter activity and expression in response to acidification (+15% activity) and warming (−30% expression) indicate some potential for short-term acclimatization, although this is probably associated with energetic trade-offs. Interestingly, whole-larvae enzyme activity (supported by abundant epidermal ionocytes) reached levels similar to those previously measured in gill tissue of adult cod, suggesting that early-life stages without functional gills are better equipped in terms of ion homeostasis than previously thought. This study implies that the gastrulation period represents a critical transition from inherited (maternal) defenses to active homeostatic regulation, which facilitates enhanced resilience of later stages to environmental factors. Article in Journal/Newspaper atlantic cod Gadus morhua Ocean acidification Alfred Wegener Institute for Polar- and Marine Research (AWI): ePIC (electronic Publication Information Center) Journal of Experimental Biology
institution Open Polar
collection Alfred Wegener Institute for Polar- and Marine Research (AWI): ePIC (electronic Publication Information Center)
op_collection_id ftawi
language unknown
description The vulnerability of fish embryos and larvae to environmental factors is often attributed to a lack of adult-like organ systems (gills) and thus insufficient homeostatic capacity. However, experimental data supporting this hypothesis are scarce. Here, by using Atlantic cod (Gadus morhua) as a model, the relationship between embryo vulnerability (to projected ocean acidification and warming) and homeostatic capacity was explored through parallel analyses of stage-specific mortality and in vitro activity and expression of major ion pumps (ATP-synthase, Na+/K+-ATPase, H+-ATPase) and co-transporters (NBC1, NKCC1). Immunolocalization of these transporters was used to study ionocyte morphology in newly hatched larvae. Treatment-related embryo mortality until hatching (+20% due to acidification and warming) occurred primarily during an early period (gastrulation) characterized by extremely low ion transport capacity. Thereafter, embryo mortality decreased in parallel with an exponential increase in activity and expression of all investigated ion transporters. Significant changes in transporter activity and expression in response to acidification (+15% activity) and warming (−30% expression) indicate some potential for short-term acclimatization, although this is probably associated with energetic trade-offs. Interestingly, whole-larvae enzyme activity (supported by abundant epidermal ionocytes) reached levels similar to those previously measured in gill tissue of adult cod, suggesting that early-life stages without functional gills are better equipped in terms of ion homeostasis than previously thought. This study implies that the gastrulation period represents a critical transition from inherited (maternal) defenses to active homeostatic regulation, which facilitates enhanced resilience of later stages to environmental factors.
format Article in Journal/Newspaper
author Dahlke, Flemming
Lucassen, Magnus
Bickmeyer, Ulf
Wohlrab, Sylke
Puvanendran, Velmurugu
Mortensen, Atle
Chierici, Melissa
Pörtner, Hans-Otto
Storch, Daniela
spellingShingle Dahlke, Flemming
Lucassen, Magnus
Bickmeyer, Ulf
Wohlrab, Sylke
Puvanendran, Velmurugu
Mortensen, Atle
Chierici, Melissa
Pörtner, Hans-Otto
Storch, Daniela
Fish embryo vulnerability to combined acidification and warming coincides with a low capacity for homeostatic regulation
author_facet Dahlke, Flemming
Lucassen, Magnus
Bickmeyer, Ulf
Wohlrab, Sylke
Puvanendran, Velmurugu
Mortensen, Atle
Chierici, Melissa
Pörtner, Hans-Otto
Storch, Daniela
author_sort Dahlke, Flemming
title Fish embryo vulnerability to combined acidification and warming coincides with a low capacity for homeostatic regulation
title_short Fish embryo vulnerability to combined acidification and warming coincides with a low capacity for homeostatic regulation
title_full Fish embryo vulnerability to combined acidification and warming coincides with a low capacity for homeostatic regulation
title_fullStr Fish embryo vulnerability to combined acidification and warming coincides with a low capacity for homeostatic regulation
title_full_unstemmed Fish embryo vulnerability to combined acidification and warming coincides with a low capacity for homeostatic regulation
title_sort fish embryo vulnerability to combined acidification and warming coincides with a low capacity for homeostatic regulation
publishDate 2020
url https://epic.awi.de/id/eprint/52355/
https://doi.org/10.1242/jeb.212589
https://hdl.handle.net/10013/epic.5507d777-665c-4936-9acc-34573911bc38
genre atlantic cod
Gadus morhua
Ocean acidification
genre_facet atlantic cod
Gadus morhua
Ocean acidification
op_source EPIC3The Journal of Experimental Biology, 223(11), pp. jeb212589, ISSN: 0022-0949
op_relation Dahlke, F. , Lucassen, M. orcid:0000-0003-4276-4781 , Bickmeyer, U. orcid:0000-0002-5351-2902 , Wohlrab, S. orcid:0000-0003-3190-0880 , Puvanendran, V. , Mortensen, A. , Chierici, M. , Pörtner, H. O. orcid:0000-0001-6535-6575 and Storch, D. orcid:0000-0003-3090-7554 (2020) Fish embryo vulnerability to combined acidification and warming coincides with a low capacity for homeostatic regulation , The Journal of Experimental Biology, 223 (11), jeb212589 . doi:10.1242/jeb.212589 <https://doi.org/10.1242/jeb.212589> , hdl:10013/epic.5507d777-665c-4936-9acc-34573911bc38
op_doi https://doi.org/10.1242/jeb.212589
container_title Journal of Experimental Biology
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