Sperm Motility Impairment in Free Spawning Invertebrates Under Near-Future Level of Ocean Acidification: Uncovering the Mechanism

Ocean acidification (OA) refers to the decrease in ocean water pH resulting from the increasing absorption of atmospheric CO2. This will cause changes in the ocean’s carbonate chemistry system with a resulting impact on reproduction of marine organisms. Reproduction is the fundamental process that a...

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Main Authors: Maria Consiglia Esposito, Raffaele Boni, Alessia Cuccaro, Elisabetta Tosti, Alessandra Gallo
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-01-01
Series:Frontiers in Marine Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmars.2019.00794/full
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author Maria Consiglia Esposito
Raffaele Boni
Alessia Cuccaro
Elisabetta Tosti
Alessandra Gallo
author_facet Maria Consiglia Esposito
Raffaele Boni
Alessia Cuccaro
Elisabetta Tosti
Alessandra Gallo
author_sort Maria Consiglia Esposito
collection DOAJ
description Ocean acidification (OA) refers to the decrease in ocean water pH resulting from the increasing absorption of atmospheric CO2. This will cause changes in the ocean’s carbonate chemistry system with a resulting impact on reproduction of marine organisms. Reproduction is the fundamental process that allows the conservation of the species; in free-spawning marine invertebrates, this process is highly sensitive to changes in seawater quality and chemistry. To date, the majority of the studies concerned OA effects on reproduction has been focused on embryo and larval development. Despite several evidence for the impairment of reproductive success by environmental perturbations through altering gamete quality, sperm physiological responses to OA are poorly investigated. In this study, we evaluated the effects of exposure to acidified seawater (AcSW) (pH 7.8), which approximate the predicted global averages for oceanic surface waters at the end of this century, on sperm quality of the mussel Mytilus galloprovincialis and the ascidian Ciona robusta by evaluating several endpoints, such as motility, vitality, mitochondrial activity, oxidative state, and intracellular pH (pHi). Following sperm exposure to AcSW, the percentage of motile spermatozoa, mitochondrial activity and pHi decreased in comparison to the current seawater pH of 8.1, whereas vitality and oxidative state were unaffected by the low external pH in both the species. In broadcast spawners, a relationship between sperm intracellular pH and the initiation of motility are well known. Spermatozoa are immotile in the testes and motility is induced after the spermatozoa are released into seawater; the alkaline pH of seawater, in fact, increases the pHi activating motility and mitochondrial respiration. The results of this study suggest that the lowering of seawater pH as predicted to occur for 2100, through the inhibition of pHi increase, prevent sperm motility activation. Sperm motility is a key determinant of fertilization success; consequently, a corresponding drop in fertilization success would be expected with important implications for the fitness and the survival of marine invertebrates.
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spelling doaj.art-bff9e06a0a3d4c7fa003ff319a7e55852022-12-21T19:00:41ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452020-01-01610.3389/fmars.2019.00794489767Sperm Motility Impairment in Free Spawning Invertebrates Under Near-Future Level of Ocean Acidification: Uncovering the MechanismMaria Consiglia Esposito0Raffaele Boni1Alessia Cuccaro2Elisabetta Tosti3Alessandra Gallo4Department of Biology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn, Naples, ItalyDepartment of Sciences, University of Basilicata, Potenza, ItalyDepartment of Biology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn, Naples, ItalyDepartment of Biology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn, Naples, ItalyDepartment of Biology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn, Naples, ItalyOcean acidification (OA) refers to the decrease in ocean water pH resulting from the increasing absorption of atmospheric CO2. This will cause changes in the ocean’s carbonate chemistry system with a resulting impact on reproduction of marine organisms. Reproduction is the fundamental process that allows the conservation of the species; in free-spawning marine invertebrates, this process is highly sensitive to changes in seawater quality and chemistry. To date, the majority of the studies concerned OA effects on reproduction has been focused on embryo and larval development. Despite several evidence for the impairment of reproductive success by environmental perturbations through altering gamete quality, sperm physiological responses to OA are poorly investigated. In this study, we evaluated the effects of exposure to acidified seawater (AcSW) (pH 7.8), which approximate the predicted global averages for oceanic surface waters at the end of this century, on sperm quality of the mussel Mytilus galloprovincialis and the ascidian Ciona robusta by evaluating several endpoints, such as motility, vitality, mitochondrial activity, oxidative state, and intracellular pH (pHi). Following sperm exposure to AcSW, the percentage of motile spermatozoa, mitochondrial activity and pHi decreased in comparison to the current seawater pH of 8.1, whereas vitality and oxidative state were unaffected by the low external pH in both the species. In broadcast spawners, a relationship between sperm intracellular pH and the initiation of motility are well known. Spermatozoa are immotile in the testes and motility is induced after the spermatozoa are released into seawater; the alkaline pH of seawater, in fact, increases the pHi activating motility and mitochondrial respiration. The results of this study suggest that the lowering of seawater pH as predicted to occur for 2100, through the inhibition of pHi increase, prevent sperm motility activation. Sperm motility is a key determinant of fertilization success; consequently, a corresponding drop in fertilization success would be expected with important implications for the fitness and the survival of marine invertebrates.https://www.frontiersin.org/article/10.3389/fmars.2019.00794/fullascidianfree spawning invertebratesmusselocean acidificationsperm qualitymotility
spellingShingle Maria Consiglia Esposito
Raffaele Boni
Alessia Cuccaro
Elisabetta Tosti
Alessandra Gallo
Sperm Motility Impairment in Free Spawning Invertebrates Under Near-Future Level of Ocean Acidification: Uncovering the Mechanism
Frontiers in Marine Science
ascidian
free spawning invertebrates
mussel
ocean acidification
sperm quality
motility
title Sperm Motility Impairment in Free Spawning Invertebrates Under Near-Future Level of Ocean Acidification: Uncovering the Mechanism
title_full Sperm Motility Impairment in Free Spawning Invertebrates Under Near-Future Level of Ocean Acidification: Uncovering the Mechanism
title_fullStr Sperm Motility Impairment in Free Spawning Invertebrates Under Near-Future Level of Ocean Acidification: Uncovering the Mechanism
title_full_unstemmed Sperm Motility Impairment in Free Spawning Invertebrates Under Near-Future Level of Ocean Acidification: Uncovering the Mechanism
title_short Sperm Motility Impairment in Free Spawning Invertebrates Under Near-Future Level of Ocean Acidification: Uncovering the Mechanism
title_sort sperm motility impairment in free spawning invertebrates under near future level of ocean acidification uncovering the mechanism
topic ascidian
free spawning invertebrates
mussel
ocean acidification
sperm quality
motility
url https://www.frontiersin.org/article/10.3389/fmars.2019.00794/full
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