Early stages of development in Mediterranean red coral (Corallium rubrum): The key role of sclerites

Corals are ecosystem engineers whose tree-like structures give three-dimensional complexity to the habitat. Their population dynamics are affected by recruitment and juvenile survival. Therefore, several defense strategies, such as the formation of hard skeletons and/or spicules, have evolved to pro...

Full description

Bibliographic Details
Main Authors: Bruna Giordano, Lorenzo Bramanti, Jonathan Perrin, Ozan Kahramanoğulları, Daniel Vielzeuf
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-02-01
Series:Frontiers in Marine Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmars.2023.1052854/full
_version_ 1811170912682115072
author Bruna Giordano
Bruna Giordano
Bruna Giordano
Lorenzo Bramanti
Jonathan Perrin
Ozan Kahramanoğulları
Daniel Vielzeuf
author_facet Bruna Giordano
Bruna Giordano
Bruna Giordano
Lorenzo Bramanti
Jonathan Perrin
Ozan Kahramanoğulları
Daniel Vielzeuf
author_sort Bruna Giordano
collection DOAJ
description Corals are ecosystem engineers whose tree-like structures give three-dimensional complexity to the habitat. Their population dynamics are affected by recruitment and juvenile survival. Therefore, several defense strategies, such as the formation of hard skeletons and/or spicules, have evolved to protect these vulnerable stages. The family Coralliidae, to which “precious corals” belong, represent an exception in the order Scleralcyonacea, as they form hard CaCO3 skeletons and small CaCO3 structures, the sclerites. The skeletogenesis of Corallium species is relatively well documented in adult colonies but remains poorly known in the early stages of the development of new colonies. To shed light on the timing of Corallium rubrum’s early skeleton formation and the role of sclerites, we focused on the first 4-years of life, applying different techniques, from scanning electron microscopy to synchrotron tomography and laser ablation inductively coupled plasma-mass spectrometry. Our results show that: 1) the first visible sclerites in the primary polyp appear at least 12 days after larval settlement, which is associated with a high CaCO3 production rate (4.5 ± 2.3 μg of CaCO3 per day). Furthermore, growth rings are visible in the sclerites, showing that fully matured sclerites grow fast, probably in 3 to 4 days. 2) Sclerites are the only biomineral product in the first year of life of C. rubrum’s colonies. 3) The evidence of a consolidated axial skeleton, intended as the inner part of the skeleton characteristic of the adult red coral (the medullary zone, MZ), is recorded for the first time in 2-year-old colonies. 4) The annular zone (AZ) around the medullary zone starts forming not before four years after settlement. Thus, primary polyp builds a deformable armor made of only sclerites during the first year. This shelter provides mechanical protection from abrasion and predation to early settled colonies. After two years, settlers are firmly and mineralogically attached to the substratum, which makes them less vulnerable to predation than younger recruits that are not anchored by the skeleton.
first_indexed 2024-04-10T17:05:42Z
format Article
id doaj.art-e54d24f30c594890a9fbc72c8241b4da
institution Directory Open Access Journal
issn 2296-7745
language English
last_indexed 2024-04-10T17:05:42Z
publishDate 2023-02-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Marine Science
spelling doaj.art-e54d24f30c594890a9fbc72c8241b4da2023-02-06T06:39:10ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452023-02-011010.3389/fmars.2023.10528541052854Early stages of development in Mediterranean red coral (Corallium rubrum): The key role of scleritesBruna Giordano0Bruna Giordano1Bruna Giordano2Lorenzo Bramanti3Jonathan Perrin4Ozan Kahramanoğulları5Daniel Vielzeuf6Department of Life and Environmental Sciences, University of Cagliari, Cagliari, ItalyDepartment of Environmental Biology, Sapienza University of Rome, Rome, ItalyLaboratoire d’Ecogéochimie des Environnements Benthiques, LECOB, Observatoire Océanologique de Banyuls sur Mer Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université, Banyuls sur Mer, FranceLaboratoire d’Ecogéochimie des Environnements Benthiques, LECOB, Observatoire Océanologique de Banyuls sur Mer Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université, Banyuls sur Mer, FranceAnatomix Beamline, Synchrotron SOLEIL, Saint Aubin, FranceFaculty of Computer Science, Free University of Bolzano-Bozen, Bolzano, ItalyAix Marseille Univ, Centre National de la Recherche Scientifique (CNRS), Centre Interdisciplinaire de Nanoscience de Marseille (CINAM), Marseille, FranceCorals are ecosystem engineers whose tree-like structures give three-dimensional complexity to the habitat. Their population dynamics are affected by recruitment and juvenile survival. Therefore, several defense strategies, such as the formation of hard skeletons and/or spicules, have evolved to protect these vulnerable stages. The family Coralliidae, to which “precious corals” belong, represent an exception in the order Scleralcyonacea, as they form hard CaCO3 skeletons and small CaCO3 structures, the sclerites. The skeletogenesis of Corallium species is relatively well documented in adult colonies but remains poorly known in the early stages of the development of new colonies. To shed light on the timing of Corallium rubrum’s early skeleton formation and the role of sclerites, we focused on the first 4-years of life, applying different techniques, from scanning electron microscopy to synchrotron tomography and laser ablation inductively coupled plasma-mass spectrometry. Our results show that: 1) the first visible sclerites in the primary polyp appear at least 12 days after larval settlement, which is associated with a high CaCO3 production rate (4.5 ± 2.3 μg of CaCO3 per day). Furthermore, growth rings are visible in the sclerites, showing that fully matured sclerites grow fast, probably in 3 to 4 days. 2) Sclerites are the only biomineral product in the first year of life of C. rubrum’s colonies. 3) The evidence of a consolidated axial skeleton, intended as the inner part of the skeleton characteristic of the adult red coral (the medullary zone, MZ), is recorded for the first time in 2-year-old colonies. 4) The annular zone (AZ) around the medullary zone starts forming not before four years after settlement. Thus, primary polyp builds a deformable armor made of only sclerites during the first year. This shelter provides mechanical protection from abrasion and predation to early settled colonies. After two years, settlers are firmly and mineralogically attached to the substratum, which makes them less vulnerable to predation than younger recruits that are not anchored by the skeleton.https://www.frontiersin.org/articles/10.3389/fmars.2023.1052854/fullCorallium rubrumearly life stagesrecruitmentbiomineralizationskeletogenesissclerites
spellingShingle Bruna Giordano
Bruna Giordano
Bruna Giordano
Lorenzo Bramanti
Jonathan Perrin
Ozan Kahramanoğulları
Daniel Vielzeuf
Early stages of development in Mediterranean red coral (Corallium rubrum): The key role of sclerites
Frontiers in Marine Science
Corallium rubrum
early life stages
recruitment
biomineralization
skeletogenesis
sclerites
title Early stages of development in Mediterranean red coral (Corallium rubrum): The key role of sclerites
title_full Early stages of development in Mediterranean red coral (Corallium rubrum): The key role of sclerites
title_fullStr Early stages of development in Mediterranean red coral (Corallium rubrum): The key role of sclerites
title_full_unstemmed Early stages of development in Mediterranean red coral (Corallium rubrum): The key role of sclerites
title_short Early stages of development in Mediterranean red coral (Corallium rubrum): The key role of sclerites
title_sort early stages of development in mediterranean red coral corallium rubrum the key role of sclerites
topic Corallium rubrum
early life stages
recruitment
biomineralization
skeletogenesis
sclerites
url https://www.frontiersin.org/articles/10.3389/fmars.2023.1052854/full
work_keys_str_mv AT brunagiordano earlystagesofdevelopmentinmediterraneanredcoralcoralliumrubrumthekeyroleofsclerites
AT brunagiordano earlystagesofdevelopmentinmediterraneanredcoralcoralliumrubrumthekeyroleofsclerites
AT brunagiordano earlystagesofdevelopmentinmediterraneanredcoralcoralliumrubrumthekeyroleofsclerites
AT lorenzobramanti earlystagesofdevelopmentinmediterraneanredcoralcoralliumrubrumthekeyroleofsclerites
AT jonathanperrin earlystagesofdevelopmentinmediterraneanredcoralcoralliumrubrumthekeyroleofsclerites
AT ozankahramanogulları earlystagesofdevelopmentinmediterraneanredcoralcoralliumrubrumthekeyroleofsclerites
AT danielvielzeuf earlystagesofdevelopmentinmediterraneanredcoralcoralliumrubrumthekeyroleofsclerites