Phytoplankton size changes and diversity loss in the southwestern Mediterranean Sea in relation to long-term hydrographic variability

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Highlights

  • Marked changes were found within phytoplankton in the SW Mediterranean from 1993 to 2008.

  • Shifts were concurrent with rising winter precipitations and SST.

  • An increase was found in the relevance of small-sized phytoplankton species.

  • A diversity loss was captured in the total phytoplankton community and diatoms.

  • Results warn on potential lesser predictable and stability ecosystem functioning.

Abstract

Structural changes in plankton primary producers have large implications for food web dynamics, energy fluxes and the vertical export of biogenic particulate carbon. Here we examine phytoplankton data spanning the period 1993–2008 from the Bay of Tunis, southwestern Mediterranean Sea, in relation to long term hydroclimate variability. We show a conspicuous shift in the structure of the phytoplankton community characterized by an increase of small-sized species and diversity loss, revealing a dominance of smaller blooming diatoms and cyanobacteria. Such changes were concurrent with marked modifications in hydroclimatic patterns experienced in the Bay of Tunis consisting of a shift towards enhanced winter precipitation together with rising temperatures. This novel study shows an overall rise in the proportion of small phytoplankton cells and a decreasing trend in phytoplankton diversity in the southern Mediterranean area. These findings warn of a potential decline of trophic efficiency and lesser food web stability resulting from mean size reduction and the diversity loss.

Introduction

Understanding how climate variability influence the dynamics of marine communities is essential to cope with climate impacts into resources management risks under scenarios of global change. Marked ecological modifications fostered by climate warming, so far documented, include (i) changes in latitude/altitude species’ ranges (Root et al., 2003), (ii) in the timing of seasonal ecological events in organism life-cycles, i.e. phenology (Edwards and Richardson, 2004), and (iii) a decrease in the mean body size of communities (Daufresne et al., 2009); the latter being considered the third universal response to warming (Peter and Sommer, 2013). Body size is a key ecological trait driving physiological processes, the dynamics of trophic interactions and energy fluxes in marine food webs. At the bottom of pelagic food webs, changes in dominant cells size further impact biogenic particulate carbon export towards the seabed, as larger phytoplankton cells sink faster than smaller ones. Hence, deciphering underlying causalities of size reduction in marine ecosystems is a current ecological challenge and a pressing endeavor in a changing world ocean.

Temperature influences phytoplankton both directly, via physiology, and indirectly, through factors controlling nutrient availability. For instance, in temperate marine ecosystems, high temperature foster stratification, thereby shaping light and nutrients availability. Indeed, recent investigations based on meta-analysis of large data sets have pointed out a leading role of resource availability in the phytoplankton size structure (Marañón et al., 2015, 2012). Likewise, mesocosms experiments have shown that temperature effects on cell size are mainly mediated by nutrient limitation (Peter and Sommer, 2013). That is, by promoting a higher stratification, warming indirectly reduce nutrients supply and primary production in surface layers, which foster a decrease of large cells along with a decline in biogenic carbon export (Chust et al., 2012; Falkowski and Oliver, 2007). The relationship between temperature and resource supply is however not trivial. It varies among ecosystems as nutrient inputs are also affected by upwelling processes, riverine discharges or even human impact. Hence, underlying factors linking warming and phytoplankton size structure are case-specific, and therefore difficult to model (Marañón et al., 2015).

To date, a number of studies have documented a significant increase in the proportion of small-sized species concurrently with warmer conditions in a variety of systems, including freshwater ( Daufresne et al., 2009), estuaries (Guinder et al., 2012) and marine ecosystems (Suikkanen et al., 2013). In the Mediterranean basin, research efforts have mainly focused on northern coasts, i.e. the Gulf of Naples (Ribera d’Alcalà et al., 2004), the central Adriatic (Mozetič et al., 2012) and the Ligurian Sea (Goffart et al., 2002; Marty et al., 2002), where phytoplankton responses to warming have shown structural changes unveiling a decline of larger cells in the community. In contrast, little is known on phytoplankton dynamics in southern coasts, although such areas may be more vulnerable to global anthropogenic changes due to the coastal concentration of anthropogenic activities due to the increasing of population density (IPCC, 2014). Furthermore, there is a lack of reports on phytoplankton variability covering recent years when Mediterranean surface waters have shown pronounced rising temperatures (Macias et al., 2013). Here, we compiled field data over the period 1993 to 2008 from a shallow ecosystem in the northern Tunisian coast, southwestern Mediterranean. We assessed hydroclimate trends, as shown by SST and precipitation, and their influence on the phytoplankton community structure, e.g. size, biomass, abundance and species shifts. We discussed on the impending consequences on phytoplankton size structure and diversity in highly productive neritic areas under projected warming scenarios in the Mediterranean Sea.

Section snippets

Methods

Hydrological features of the Bay of Tunis are influenced by the inflowing Atlantic waters in the northernmost part (Millot, 1999), whereas the southern area is characterized by shallow, eutrophic coastal lagoons (Supplementary Information SI Fig. 1) (Daly Yahia-Kéfi et al., 2005). The nutrient dynamics shows a zonal trophic gradient from the eutrophic southwestern region to the mesotrophic northeastern area (Souissi et al., 2000).

Results

The annual pattern of salinity displayed average values of 36.34 ± 2.61, with maximum reached 38–38.8 in August, while minimum values, approx. 26.6–27, were registered during rainy periods (from September to June). In turn, the annual pattern of SST showed an average of 19.6 °C ± 4.2, although during the last years of series (2005–2009) an upward trend was observed (Fig. 1 a, Table 1). Regional climate drivers in this shallow ecosystem, SST and winter precipitation (DJFM) showed statistical

Discussion

We have investigated temporal changes in phytoplankton in the northern Tunisian coast. The analysis revealed structural changes in the phytoplankton community, which shifted towards a dominance of smaller cells along with a loss of diversity.

Conclusions

Our results show conspicuous shifts in the structure of phytoplankton communities likely fostered by the compound effects of rising precipitation and temperatures experienced in the Bay of Tunis during the last decades. The observed changes in the structure of phytoplankton community suggest a reorganization in the plankton food web. Hence, southern Mediterranean warming projections, together with anthropogenic nutrient inputs warn on the high vulnerability these ecosystems experience to

Author contributions

We state the manuscript is original and is not submitted elsewhere. All the listed authors are in agreement and approve the submitted version. NS, OK-DY and MNDY leaded the sampling and field data analysis. E R-R, JCM and US conceived this study and performed the statistical analysis of the results. All the authors contributed during the writing and revision of the manuscript.

Declaration of competing interest

None.

Acknowledgements

We gratefully acknowledge the support of the European Commission: OCEAN-CERTAIN (FP7-ENV-2013-6.1-1; no: 603773). Eduardo Ramirez Romero thanks the funding from “Govern de les Illes Balears—Conselleria d’Innovació, Recerca i Turisme, Programa Vicenç Mut.”

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