Ultradian rhythms in shell composition of photosymbiotic and non-photosymbiotic mollusks

Niels J. De Winter*, Daniel Killam, Lukas Fröhlich, Lennart De Nooijer, Wim Boer, Bernd R. Schöne, Julien Thébault, Gert Jan Reichart

*Corresponding author for this work

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

The chemical composition of mollusk shells is a useful tool in (paleo)climatology since it captures inter- and intra-annual variability in environmental conditions. Trace element and stable isotope analysis with improved sampling resolution now allows in situ determination of the composition of mollusk shell volumes precipitated at daily to sub-daily time intervals. Here, we discuss hourly resolved Mg / Ca, Mn / Ca, Sr / Ca, and Ba / Ca profiles measured by laser ablation inductively coupled plasma - mass spectrometry (ICP-MS) through shells of the photosymbiotic giant clams (Tridacna maxima, T. squamosa, and T. squamosina) and the non-photosymbiotic scallop Pecten maximus. Precise sclerochronological age models and spectral analysis allowed us to extract daily and tidal rhythms in the trace element composition of these shells. We find weak but statistically significant expressions of these periods and conclude that this cyclicity explains less than 10 % of the sub-annual variance in trace element profiles. Tidal and diurnal rhythms explain variability of, at most, 0.2 mmol mol-1 (∼10 % of mean value) in Mg / Ca and Sr / Ca, while ultradian Mn / Ca and Ba / Ca cyclicity has a median amplitude of less than 2 μmol mol-1 mol mol-1 (∼40 % and 80 % of the mean of Mn / Ca and Ba / Ca, respectively). Daily periodicity in Sr / Ca and Ba / Ca is stronger in Tridacna than in Pecten, with Pecten showing stronger tidal periodicity. One T. squamosa specimen which grew under a sunshade exhibits among the strongest diurnal cyclicity. Daily cycles in the trace element composition of giant clams are therefore unlikely to be driven by variations in direct insolation but rather reflect an inherent biological rhythmic process affecting element incorporation. Finally, the large amount of short-term trace element variability unexplained by tidal and daily rhythms highlights the dominance of aperiodic processes in mollusk physiology and/or environmental conditions over shell composition at the sub-daily scale. Future studies should aim to investigate whether this remaining variability in shell chemistry reliably records weather patterns or circulation changes in the animals' environment.

Original languageEnglish
Pages (from-to)3027-3052
Number of pages26
JournalBiogeosciences
Volume20
Issue number14
Early online date28 Jul 2023
DOIs
Publication statusPublished - 2023

Bibliographical note

Funding Information:
The authors would like to thank Leonard Bik for his help with the sample preparation and Maarten Zeilmans for his help with the high-resolution imaging of the samples at Utrecht University. This study is part of the UNBIAS project, jointly funded by the Flemish Research Foundation (FWO; grant no. 12ZB220N) post-doctoral fellowship (Niels J. de Winter) and a Marie Skłodowska-Curie Actions (MSCA) Individual Fellowship (grant nos. H2020-MSCA-IF-2018, 843011 – UNBIAS; awarded to Niels J. de Winter). Gert-Jan Reichart and Lennart de Nooijer acknowledge funding from the Netherlands Earth System Science Center (NESSC; grant no. 024.002.001) from the Dutch Ministry for Education, Culture and Science (gravitation grant no. NWO 024.002.001). Bernd R. Schöne acknowledges funding from the Deutsche Forschungsgemeinschaft (DFG; grant nos. SCHO 793/21 (HIPPO) and SCHO 793/23). Julien Thébault was funded by the French National Research Agency (ANR; grant no. ANR-18-CE92-0036-01) awarded within the framework of the French-German collaborative project HIPPO (HIgh-resolution Primary Production multiprOxy archives).

Funding Information:
This research has been supported by the European Commission, Horizon 2020 Framework Programme (UNBIAS (grant nos. H2020-MSCA-IF-2018, 843011)); the Fonds Wetenschappelijk Onderzoek (grant no. 12ZB220N); the Aard- en Levenswetenschappen, Nederlandse Organisatie voor Wetenschappelijk Onderzoek (grant no. 024.002.001); the Deutsche Forschungsgemeinschaft (grant nos. SCHO/793/21 and SCHO 793/23); and the Agence Nationale de la Recherche (grant no. ANR-18-CE92-0036-01).

Publisher Copyright:
© Copyright:

Funding

The authors would like to thank Leonard Bik for his help with the sample preparation and Maarten Zeilmans for his help with the high-resolution imaging of the samples at Utrecht University. This study is part of the UNBIAS project, jointly funded by the Flemish Research Foundation (FWO; grant no. 12ZB220N) post-doctoral fellowship (Niels J. de Winter) and a Marie Skłodowska-Curie Actions (MSCA) Individual Fellowship (grant nos. H2020-MSCA-IF-2018, 843011 – UNBIAS; awarded to Niels J. de Winter). Gert-Jan Reichart and Lennart de Nooijer acknowledge funding from the Netherlands Earth System Science Center (NESSC; grant no. 024.002.001) from the Dutch Ministry for Education, Culture and Science (gravitation grant no. NWO 024.002.001). Bernd R. Schöne acknowledges funding from the Deutsche Forschungsgemeinschaft (DFG; grant nos. SCHO 793/21 (HIPPO) and SCHO 793/23). Julien Thébault was funded by the French National Research Agency (ANR; grant no. ANR-18-CE92-0036-01) awarded within the framework of the French-German collaborative project HIPPO (HIgh-resolution Primary Production multiprOxy archives). This research has been supported by the European Commission, Horizon 2020 Framework Programme (UNBIAS (grant nos. H2020-MSCA-IF-2018, 843011)); the Fonds Wetenschappelijk Onderzoek (grant no. 12ZB220N); the Aard- en Levenswetenschappen, Nederlandse Organisatie voor Wetenschappelijk Onderzoek (grant no. 024.002.001); the Deutsche Forschungsgemeinschaft (grant nos. SCHO/793/21 and SCHO 793/23); and the Agence Nationale de la Recherche (grant no. ANR-18-CE92-0036-01).

FundersFunder number
Netherlands Earth System Science Centre
European Commission, Horizon 2020 Framework Programme
Aard- en Levenswetenschappen
UNBIAS
H2020 Marie Skłodowska-Curie ActionsH2020-MSCA-IF-2018, 843011
Fonds Wetenschappelijk Onderzoek12ZB220N
Nederlandse Organisatie voor Wetenschappelijk Onderzoek024.002.001
Agence Nationale de la RechercheANR-18-CE92-0036-01
Horizon 2020 Framework Programme844909
Deutsche ForschungsgemeinschaftSCHO/793/21, SCHO 793/23
Dutch Ministry for Education, Culture and ScienceNWO 024.002.001

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