Brooding in the Chilean oyster Ostrea chilensis: unexpected complexity in the movements of brooded offspring within the mantle cavity.

Brooding in invertebrates serves to protect embryos from stressful external conditions by retaining progeny inside the female body, effectively reducing the risk of pelagic stages being exposed to predation or other environmental stressors, but with accompanying changes in pallial fluid characterist...

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Main Authors: Daniela A Mardones-Toledo, Jaime A Montory, Alyssa Joyce, Raymond J Thompson, Casey M Diederich, Jan A Pechenik, Maria L Mardones, Oscar R Chaparro
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0122859
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spelling doaj-42f9498576c848d6b957736d233484462021-03-03T20:06:23ZengPublic Library of Science (PLoS)PLoS ONE1932-62032015-01-01104e012285910.1371/journal.pone.0122859Brooding in the Chilean oyster Ostrea chilensis: unexpected complexity in the movements of brooded offspring within the mantle cavity.Daniela A Mardones-ToledoJaime A MontoryAlyssa JoyceRaymond J ThompsonCasey M DiederichJan A PechenikMaria L MardonesOscar R ChaparroBrooding in invertebrates serves to protect embryos from stressful external conditions by retaining progeny inside the female body, effectively reducing the risk of pelagic stages being exposed to predation or other environmental stressors, but with accompanying changes in pallial fluid characteristics, including reduced oxygen availability. Brooded embryos are usually immobile and often encapsulated, but in some Ostrea species the embryos move freely inside the female pallial cavity in close association with the mother's gills for as long as eight weeks. We used endoscopic techniques to characterize the circulation pattern of embryos brooded by females of the oyster, Ostrea chilensis. Progeny at embryonic and veliger stages typically circulated in established patterns that included the use of dorsal and ventral food grooves (DFG, VFG) to move anteriorly on the gills. Both embryos and veligers accumulated around the mother's palps, and remained there until an active maternal countercurrent moved them to the gill inhalant area. Both food grooves were able to move embryos, veligers, and food-particle aggregates anteriorly, but the DFG was more important in progeny transport; early embryos were moved more rapidly than veligers in the DFG. A microcirculation pattern of embryos was apparent when they were moved by gill lamellae: when they were close to the VFG, most embryos lost gill contact and "fell" down to the DFG. Those that actually reached the DFG moved anteriorly, but others came into contact with the base of the lamellae and again moved towards the VFG. The circulation pattern of the progeny appears well-suited for both cleaning them and directing them posteriorly to an area where there is more oxygen and food than in the palp region. This process for actively circulating progeny involves the feeding structures (gill and palps) and appears to be energetically costly for the female. It also interferes with feeding, which could explain the poor energy balance previously documented for brooding females of this species.https://doi.org/10.1371/journal.pone.0122859
collection DOAJ
language English
format Article
sources DOAJ
author Daniela A Mardones-Toledo
Jaime A Montory
Alyssa Joyce
Raymond J Thompson
Casey M Diederich
Jan A Pechenik
Maria L Mardones
Oscar R Chaparro
spellingShingle Daniela A Mardones-Toledo
Jaime A Montory
Alyssa Joyce
Raymond J Thompson
Casey M Diederich
Jan A Pechenik
Maria L Mardones
Oscar R Chaparro
Brooding in the Chilean oyster Ostrea chilensis: unexpected complexity in the movements of brooded offspring within the mantle cavity.
PLoS ONE
author_facet Daniela A Mardones-Toledo
Jaime A Montory
Alyssa Joyce
Raymond J Thompson
Casey M Diederich
Jan A Pechenik
Maria L Mardones
Oscar R Chaparro
author_sort Daniela A Mardones-Toledo
title Brooding in the Chilean oyster Ostrea chilensis: unexpected complexity in the movements of brooded offspring within the mantle cavity.
title_short Brooding in the Chilean oyster Ostrea chilensis: unexpected complexity in the movements of brooded offspring within the mantle cavity.
title_full Brooding in the Chilean oyster Ostrea chilensis: unexpected complexity in the movements of brooded offspring within the mantle cavity.
title_fullStr Brooding in the Chilean oyster Ostrea chilensis: unexpected complexity in the movements of brooded offspring within the mantle cavity.
title_full_unstemmed Brooding in the Chilean oyster Ostrea chilensis: unexpected complexity in the movements of brooded offspring within the mantle cavity.
title_sort brooding in the chilean oyster ostrea chilensis: unexpected complexity in the movements of brooded offspring within the mantle cavity.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2015-01-01
description Brooding in invertebrates serves to protect embryos from stressful external conditions by retaining progeny inside the female body, effectively reducing the risk of pelagic stages being exposed to predation or other environmental stressors, but with accompanying changes in pallial fluid characteristics, including reduced oxygen availability. Brooded embryos are usually immobile and often encapsulated, but in some Ostrea species the embryos move freely inside the female pallial cavity in close association with the mother's gills for as long as eight weeks. We used endoscopic techniques to characterize the circulation pattern of embryos brooded by females of the oyster, Ostrea chilensis. Progeny at embryonic and veliger stages typically circulated in established patterns that included the use of dorsal and ventral food grooves (DFG, VFG) to move anteriorly on the gills. Both embryos and veligers accumulated around the mother's palps, and remained there until an active maternal countercurrent moved them to the gill inhalant area. Both food grooves were able to move embryos, veligers, and food-particle aggregates anteriorly, but the DFG was more important in progeny transport; early embryos were moved more rapidly than veligers in the DFG. A microcirculation pattern of embryos was apparent when they were moved by gill lamellae: when they were close to the VFG, most embryos lost gill contact and "fell" down to the DFG. Those that actually reached the DFG moved anteriorly, but others came into contact with the base of the lamellae and again moved towards the VFG. The circulation pattern of the progeny appears well-suited for both cleaning them and directing them posteriorly to an area where there is more oxygen and food than in the palp region. This process for actively circulating progeny involves the feeding structures (gill and palps) and appears to be energetically costly for the female. It also interferes with feeding, which could explain the poor energy balance previously documented for brooding females of this species.
url https://doi.org/10.1371/journal.pone.0122859
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