Diel patterns of microphytobenthic primary production in intertidal sediments: the role of photoperiod on the vertical migration circadian rhythm

S. Haro,A. Corzo,C. J. González,J. M. Crespo,E. Garcia-Robledo,J. Bohórquez,S. Papaspyrou,M. Lara

doi:10.1038/s41598-019-49971-8

S. Haro, A. Corzo + Show 6 more

Open Access

https://doi.org/10.1038/s41598-019-49971-8

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Abstract

Diel primary production patterns of intertidal microphytobenthos (MPB) have been attributed to short-term physiological changes in the photosynthetic apparatus or to diel changes in the photoautotrophic biomass in the sediment photic layer due to vertical migration. Diel changes in primary production and vertical migration are entrained by external factors like photoperiod and tides. However, the role of photoperiod and tides has not been experimentally separated to date. Here, we performed laboratory experiments with sediment cores kept in immersion, in the absence of tides, with photoperiod or under continuous light. Measurements of net production, made with O2 microsensors, and of spectral reflectance at the sediment surface showed that, in intertidal sediments, the photoperiod signal was the major driver of the diel patterns of net primary production and sediment oxygen availability through the vertical migration of the MPB photoautotrophic biomass. Vertical migration was controlled by an endogenous circadian rhythm entrained by photoperiod in the absence of tides. The pattern progressively disappeared after 3 days in continuous light but was immediately reset by photoperiod. Even though a potential contribution of a subjective in situ tidal signal cannot be completely discarded, Fourier and cross spectral analysis of temporal patterns indicated that the photosynthetic circadian rhythm was mainly characterized by light/dark migratory cycles.

Highlights

Intertidal sediments are a complex environment where strong physicochemical changes occur at different spatiotemporal scales, i.e. diel photoperiod and tidal cycles, fortnight tidal cycles, and seasonal changes[1]
Diel changes of photosynthesis rate in many primary producers, from cyanobacteria to higher plants are endogenously controlled by circadian rhythms, endogenous biological clocks that time metabolic, physiological and behaviour events to the diel cycle[18,19,20,21,22]
Photosynthetic circadian rhythms are controlled through the regulation of different components of the photosynthetic apparatus in different species and taxonomic groups[19,21,27,28,29]

Summary

Introduction

Intertidal sediments are a complex environment where strong physicochemical changes occur at different spatiotemporal scales, i.e. diel photoperiod and tidal cycles, fortnight tidal cycles (spring-neap tides), and seasonal changes[1]. We show that diel oscillations of net primary production in intertidal sediments, measured by O2 microsensors, can occur in the absence of tides due to the vertical migration of photoautotrophic biomass (estimated by spectral reflectance) This migration is under the control of a circadian rhythm entrained by the photoperiod signal, even though the contribution of other environmental clues, like the subjective tidal cycle cannot be potentially discarded. This oscillatory diel pattern in primary production has practical implication for the precise measurement of daily and seasonal rates and it has deep ecological and biogeochemical implications, regarding the coupling between the photoautotrophic and heterotrophic communities, the sediment net metabolism and the rate and pathway of organic matter mineralization

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