Photoperiod-driven rhythms reveal multi-decadal stability of phytoplankton communities in a highly fluctuating coastal environment

Abstract

Phytoplankton play a pivotal role in global biogeochemical and trophic processes and provide essential ecosystem services. However, there is still no broad consensus on how and to what extent their community composition responds to environmental variability. Here, high-frequency oceanographic and biological data collected over more than 25 years in a coastal Mediterranean site are used to shed light on the temporal patterns of phytoplankton species and assemblages in their environmental context. Because of the proximity to the coast and due to large-scale variations, environmental conditions showed variability on the short and long-term scales. Nonetheless, an impressive regularity characterised the annual occurrence of phytoplankton species and their assemblages, which translated into their remarkable stability over decades. Photoperiod was the dominant factor related to community turnover and replacement, which points at a possible endogenous regulation of biological processes associated with species-specific phenological patterns, in analogy with terrestrial plants. These results highlight the considerable stability and resistance of phytoplankton communities in response to different environmental pressures, which contrast the view of these organisms as passively undergoing changes that occur at different temporal scales in their habitat, and show how, under certain conditions, biological processes may prevail over environmental forcing.

Temporal changes of genetic structure and diversity in a marine diatom genus discovered via metabarcoding

“…To correct the attribution of ambiguous ancillary haplotypes, we assume that all haplotypes belonging to the same taxon, that is, to the same population of freely interbreeding individuals, share a comparable distribution of reads over the sample dates. This expectation is supported by the marked seasonality of the Pseudo-nitzschia species observed in this study, as already found in previous studies based on environmental clone libraries (McDonald et al, 2007;Ruggiero et al, 2015) and on the analysis of the whole phytoplankton community (Longobardi et al, 2022) in the GoN.…”

Phenological segregation suggests speciation by time in the planktonic diatom Pseudo‐nitzschia allochrona sp. nov.

“…Yet, phenology, that is, the seasonal time window of species' occurrences, has rarely been considered a stable, endogenous character in phytoplankton, whereby the alternation of different species over the seasons is postulated to be strictly driven by changes in environmental conditions. Nevertheless, annually recurrent patterns are seen in long‐term analysis of nano‐ and microphytoplankton species of the Gulf of Naples, where photoperiod is the most important explanatory variable driving community turnover (Longobardi et al, 2022 ; Ribera d'Alcalà et al, 2004 ). Recent massive eDNA sequencing from other areas has also revealed recurrent occurrence of picoplanktonic taxa against marked environmental variability (Giner et al, 2019 ; Lambert et al, 2019 ), which can be explained based on endogenous rhythms and stability of phenological characteristics.…”

“…Nevertheless, annually recurrent patterns are seen in long-term analysis of nano-and microphytoplankton species of the Gulf of Naples, where photoperiod is the most important explanatory variable driving community turnover (Longobardi et al, 2022;Ribera d'Alcalà et al, 2004) The mechanisms underlying allochronic speciation, and speciation in general, are not easy to clarify (Orsini et al, 2013), as both neutral and selective processes could be involved. Time and environmental variables covary, making it difficult to discern their respective contribution to the patterns observed in this study.…”

Insight into diatoms diversity at two European coastal sites (LTER-MC in the Mediterranean Sea and SOMLIT-Astan in the Western English Channel) using a DNA Metabarcoding approach

“…In fact, the observed dynamics in read relative abundance results from many different processes affecting either cell growth or cell losses via diverse mechanisms (for example, sedimentation, grazing, programmed cell death, internal clock, or infection by parasites). The synchronic variations in read contribution to total counts in such different and geographically distant sites could indicate that internal controls of growth rate and sexual reproduction, rather that external environmental parameters are at work (Cianelli et al, 2017; D’Alelio et al, 2010; Jewson et al, 2016; Longobardi et al 2022). The 4 other species, identified as core and abundant in the 2 sites, may be more adapted to respond to natural environmental variability, and take advantage, for example, of pulses of nutrients.…”