Comprehensive model of annual plankton succession based on the whole-plankton time series approach

Abstract

Ecological succession provides a widely accepted description of seasonal changes in phytoplankton and mesozooplankton assemblages in the natural environment, but concurrent changes in smaller (i.e. microbes) and larger (i.e. macroplankton) organisms are not included in the model because plankton ranging from bacteria to jellies are seldom sampled and analyzed simultaneously. Here we studied, for the first time in the aquatic literature, the succession of marine plankton in the whole-plankton assemblage that spanned 5 orders of magnitude in size from microbes to macroplankton predators (not including fish or fish larvae, for which no consistent data were available). Samples were collected in the northwestern Mediterranean Sea (Bay of Villefranche) weekly during 10 months. Simultaneously collected samples were analyzed by flow cytometry, inverse microscopy, FlowCam, and ZooScan. The whole-plankton assemblage underwent sharp reorganizations that corresponded to bottom-up events of vertical mixing in the water-column, and its development was top-down controlled by large gelatinous filter feeders and predators. Based on the results provided by our novel whole-plankton assemblage approach, we propose a new comprehensive conceptual model of the annual plankton succession (i.e. whole plankton model) characterized by both stepwise stacking of four broad trophic communities from early spring through summer, which is a new concept, and progressive replacement of ecological plankton categories within the different trophic communities, as recognised traditionally.

Fig 1. Map of the study area showing the general circulation in the Ligurian basin (black arrows).

The peripheral zone (Pz), the frontal zone (Fz), schematized as a box superimposed on the top black arrow, and the central zone (Cz) are represented. LC stands for Ligurian Current. Bathymetric map of the Bay of Villefranche with the sampling station Point B (43°41.10 N, 7°19.00 E).

Fig 2. 18 Plankton Ecological Categories, PECs (abbreviations), symbols, and ecological traits.

The symbols used as visual aid in the figures.

Fig 3. Variations of environmental conditions at the sampling station between December 2010 and October 2011.

The two coloured bars at the top represent the duration of the different clusters based on the two sets of variables, i.e. physical (W = winter, SP = spring, T = transition, S1 = summer 1, S2 = summer 2) and biological (W = winter, ES = early spring, LS1 = late spring 1, LS2 = Late Spring 2, S = summer) (the clustering analyses are detailed in Fig. 4). Panels: (a) temperature, (b) salinity, (c) water density with (indicated below) periods of mixing (M1–M4) and stability (ST1-ST4), (d) nitrate, and (e) silicate. The white dotted curve repeated in all panels represents the depth of the maximum density gradient (pycnocline) estimated from the Brunt-Vaïsälä frequency. The vertical lines represent the limits of clusters based on biological variables (i.e. PEC time series).

Fig 4. Cluster analyses of physical (temperature and salinity, left) and biological (PEC biovolumes, right) data.

Three significant clustering levels were identified for the physical characteristics of the water column: level P1, (cut-off = 11, red and blue branches of the tree); level P2 (cut-off = 8.6, solid-line coloured rectangles); level P3 (cut-off = 5.8, dashed-line coloured rectangles). Four significant clustering levels were identified for the biological data: level B1 (cut-off = 3.71, red and blue branches of the tree); level B2 (cut-off = 3.28, solid-line coloured rectangles); level B3 (cut-off = 2.89, dashed-line rectangles) which clustered 4 groups; level B4 (cut-off = 2.89, coloured fonts) which clustered 5 groups.

Fig 5. Time series of PEC biovolumes at the sampling station from December 2010 to October 2011.

The top coloured bars represent the periods identified from the clustering analyses based on physical and biological variables (coloured bars as in Fig. 3). The vertical dashed lines represent limits of clusters based on biological variables (i.e. PEC time series). Red dashes under the x-axes represent mixing events (see Fig. 3). Note the different scales on the y-axes.

Fig 6. Conceptual representation of the whole-plankton model.

The top coloured bar represents the periods identified from the clustering analysis based on biological variables (i.e. PEC time series; coloured bar as in Fig. 3). Each trophic community is represented in a horizontal box, and the boxes are stacking up from bottom to top. In the primary producers and grazers boxes, the black arrows represent the traditional replacement-based ecological succession. The stacking of trophic boxes represents the stacking of trophic level occurring over the course of the succession. Each group of organisms depicted here is defined in Fig. 2. The bottom bars identify the periods of vertical mixing and stability of the water column.