Antagonistic Interactions and Clutch-Dependent Sensitivity Induce Variable Responses to Ocean Acidification and Warming in Squid (Doryteuthis pealeii) Embryos and Paralarvae

Ocean acidification (OA) and warming seas are significant concerns for coastal systems and species. The Atlantic longfin squid, Doryteuthis pealeii, a core component of the Northwest Atlantic trophic web, has demonstrated impacts, such as reduced growth and delayed development, under high chronic ex...

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Main Authors: Casey J. Zakroff, T. Aran Mooney
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-05-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fphys.2020.00501/full
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author Casey J. Zakroff
Casey J. Zakroff
T. Aran Mooney
author_facet Casey J. Zakroff
Casey J. Zakroff
T. Aran Mooney
author_sort Casey J. Zakroff
collection DOAJ
description Ocean acidification (OA) and warming seas are significant concerns for coastal systems and species. The Atlantic longfin squid, Doryteuthis pealeii, a core component of the Northwest Atlantic trophic web, has demonstrated impacts, such as reduced growth and delayed development, under high chronic exposure to acidification (2200 ppm), but the combined effects of OA and warming have not been explored in this species. In this study, D. pealeii egg capsules were reared under a combination of several acidification levels (400, 2200, and 3500 ppm) and temperatures (20 and 27°C). Hatchlings were measured for a range of metrics [dorsal mantle length (DML), yolk sac volume (YV), malformation, and hatching success] in three trials over the 2016 breeding season (May – October). Although notable resistance to stressors was seen, highlighting variability within and between clutches, reduced DML and malformation of the embryos occurred at the highest OA exposure. Surprisingly, increased temperatures did not appear to exacerbate OA impacts, although responses were variable. Time to hatching, which increased with acidification, decreased much more drastically under warming and, further, decreased or removed delays caused by acidification. Hatching success, while variable by clutch, showed consistent patterns of greater late stage loss of embryos under acidification and greater early stage loss under warming, highlighting the potential difference in timing between these stressors for this system, i.e., that acidification stress builds up and causes impacts over time within the egg capsule as the embryos grow and respire. High OA-exposed hatchlings from the warmer conditions often showed reduced impacts compared to those reared in ambient temperatures. This may be due to the increased developmental rate and subsequently reduced OA exposure time of embryos in the higher temperature treatment. These results indicate a substantive potential plasticity to multiple stressors during the embryonic development of this species of squid, but do not predict how this species would fare under these future ocean scenarios.
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spelling doaj.art-119d2f49be4e43219b1873d53167301c2022-12-21T22:41:35ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2020-05-011110.3389/fphys.2020.00501481381Antagonistic Interactions and Clutch-Dependent Sensitivity Induce Variable Responses to Ocean Acidification and Warming in Squid (Doryteuthis pealeii) Embryos and ParalarvaeCasey J. Zakroff0Casey J. Zakroff1T. Aran Mooney2Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, United StatesMassachusetts Institute of Technology–Woods Hole Oceanographic Institution Joint Program in Oceanography/Applied Ocean Science and Engineering, Cambridge, MA, United StatesBiology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, United StatesOcean acidification (OA) and warming seas are significant concerns for coastal systems and species. The Atlantic longfin squid, Doryteuthis pealeii, a core component of the Northwest Atlantic trophic web, has demonstrated impacts, such as reduced growth and delayed development, under high chronic exposure to acidification (2200 ppm), but the combined effects of OA and warming have not been explored in this species. In this study, D. pealeii egg capsules were reared under a combination of several acidification levels (400, 2200, and 3500 ppm) and temperatures (20 and 27°C). Hatchlings were measured for a range of metrics [dorsal mantle length (DML), yolk sac volume (YV), malformation, and hatching success] in three trials over the 2016 breeding season (May – October). Although notable resistance to stressors was seen, highlighting variability within and between clutches, reduced DML and malformation of the embryos occurred at the highest OA exposure. Surprisingly, increased temperatures did not appear to exacerbate OA impacts, although responses were variable. Time to hatching, which increased with acidification, decreased much more drastically under warming and, further, decreased or removed delays caused by acidification. Hatching success, while variable by clutch, showed consistent patterns of greater late stage loss of embryos under acidification and greater early stage loss under warming, highlighting the potential difference in timing between these stressors for this system, i.e., that acidification stress builds up and causes impacts over time within the egg capsule as the embryos grow and respire. High OA-exposed hatchlings from the warmer conditions often showed reduced impacts compared to those reared in ambient temperatures. This may be due to the increased developmental rate and subsequently reduced OA exposure time of embryos in the higher temperature treatment. These results indicate a substantive potential plasticity to multiple stressors during the embryonic development of this species of squid, but do not predict how this species would fare under these future ocean scenarios.https://www.frontiersin.org/article/10.3389/fphys.2020.00501/fullcephalopodhypercapniaMyopsidatemperaturestressmultifactor
spellingShingle Casey J. Zakroff
Casey J. Zakroff
T. Aran Mooney
Antagonistic Interactions and Clutch-Dependent Sensitivity Induce Variable Responses to Ocean Acidification and Warming in Squid (Doryteuthis pealeii) Embryos and Paralarvae
Frontiers in Physiology
cephalopod
hypercapnia
Myopsida
temperature
stress
multifactor
title Antagonistic Interactions and Clutch-Dependent Sensitivity Induce Variable Responses to Ocean Acidification and Warming in Squid (Doryteuthis pealeii) Embryos and Paralarvae
title_full Antagonistic Interactions and Clutch-Dependent Sensitivity Induce Variable Responses to Ocean Acidification and Warming in Squid (Doryteuthis pealeii) Embryos and Paralarvae
title_fullStr Antagonistic Interactions and Clutch-Dependent Sensitivity Induce Variable Responses to Ocean Acidification and Warming in Squid (Doryteuthis pealeii) Embryos and Paralarvae
title_full_unstemmed Antagonistic Interactions and Clutch-Dependent Sensitivity Induce Variable Responses to Ocean Acidification and Warming in Squid (Doryteuthis pealeii) Embryos and Paralarvae
title_short Antagonistic Interactions and Clutch-Dependent Sensitivity Induce Variable Responses to Ocean Acidification and Warming in Squid (Doryteuthis pealeii) Embryos and Paralarvae
title_sort antagonistic interactions and clutch dependent sensitivity induce variable responses to ocean acidification and warming in squid doryteuthis pealeii embryos and paralarvae
topic cephalopod
hypercapnia
Myopsida
temperature
stress
multifactor
url https://www.frontiersin.org/article/10.3389/fphys.2020.00501/full
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