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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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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