Shifts in phytoplankton community structure across oceanic boundaries

Abstract

Phytoplankton communities play an important role in marine food webs and biogeochemical cycles. The transition zones between ocean gyres and surrounding waters represent critical ecological boundaries where environmental gradients drive significant shifts in phytoplankton community structure. This study investigates how nutrient availability and temperature shape the size distribution and composition of small phytoplankton (< 5 [Formula: see text]m) communities across the North Pacific Subtropical Gyre (NPSG) boundaries, testing several ecological hypotheses that explain phytoplankton size distribution patterns in relation to environmental variability. We used high-resolution, underway flow cytometry data collected during eight oceanographic cruises from 2016 to 2021 to assess changes in phytoplankton biomass and growth rate across the gyre boundaries. The cyanobacterium Prochlorococcus dominated within the gyre, with biomass ranging from 3.2 to 13.1 [Formula: see text]gC L-1, and its relative contribution to total phytoplankton biomass varied among cruises (31% to 81%, average 60 [Formula: see text] 16%). Prochlorococcus growth rates were significantly higher within the gyre (0.43 [Formula: see text] 0.18 per day) than outside the gyre (0.28 [Formula: see text] 0.16 per day) (one-sided t-test, p < 0.001). Northward in the gyre, Prochlorococcus biomass and growth rates declined. Some variations in biomass and growth rates were observed southward and eastward, with biomass ranging from 3 to 10 [Formula: see text]gC L-1 and growth rate ranging from 0.2 to 0.6 per day. Outside the NPSG, total phytoplankton biomass increased, with nanoeukaryotes becoming the predominant contributors (up to 71%, 9.1 [Formula: see text] 7.3 [Formula: see text]gC L-1). Picoeukaryote biomass also increased outside the gyre (up to 28 [Formula: see text] 12% of total biomass). Nutrient concentrations increased by nearly two orders of magnitude outside the NPSG, coinciding with the shift towards larger phytoplankton. The dominance of Prochlorococcus within the gyre emphasizes its adaptation to oligotrophic conditions, while the shift towards larger size classes outside the gyre likely reflects the relatively higher nutrient availability. The relatively low abundance of Synechococcus even in nutrient-rich regions suggest that that factors beyond nutrient availability, such as grazing, may influence its distribution. These findings have implications for understanding how phytoplankton communities will respond to future changes in oceanographic conditions, such as warming and altered nutrient regimes.

Fig 1. Environmental gradients and nutrient distributions across distance from the gyre boundary.

(a) Cruise tracks, with each colored line representing a different cruise, with some cruises overlapping in certain regions (i.e., NSP1, dark green, NSP2, green, NSP3, light green, and NSU2, pink, in the north). (b) Salinity (PSU) and (c) temperature (°C) along each cruise track, plotted as a function of distance (km) from the gyre boundary. (d) Each cruise was divided into three regions based on change in salinity (see Methods): the NPSG (purple), the gyre boundary (yellow), and the region outside the NPSG (teal). (e) Dissolved inorganic nitrogen (DIN) and (f) dissolved inorganic phosphorus (DIP) concentrations ($\mu$mol L⁻¹) along each cruise track. Negative distances indicate locations inside the gyre, while positive distances represent locations outside the gyre. along each cruise track. Error bars in c) and d) represent standard deviations of the binned data over 100 km intervals (average N = 10 per bin). The gray shaded area highlights the gyre boundary.

Fig 2. Phytoplankton biomass and cell abundance across distance from the gyre boundary

a) Phytoplankton biomass ($\mu$g C L⁻¹) and b) cell abundance (10⁶cells L⁻¹) relative to distance (km) from the gyre boundary (grey bar), with negative distances indicating locations within the gyre and positive distances representing locations outside the gyre. Colored lines represent the biomass of different phytoplankton groups: Prochlorococcus (orange), Synechococcus (red), picoeukaryotes (<2 $\mu$m, purple), nanoeukaryotes (2-5 $\mu$m, black). Prochlorococcus abundance drops below detection during NSU1 and NSU2 outside the gyre. Error bars in b) represent standard deviations of the binned data over 100 km intervals (N = 1-7 per bin, average N = 2). The gray shaded area highlights the gyre boundary.

Fig 3. Phytoplankton cell size across distance from the gyre boundary.

Phytoplankton cell size ($\mu$m ESD, equivalent spherical diameter) plotted against distance (km) from the gyre boundary (grey bar), with negative distances indicating locations within the gyre and positive distances representing locations outside the gyre. Colored lines represent the biomass of different phytoplankton groups: Prochlorococcus (orange), Synechococcus (red), picoeukaryotes (<2 $\mu$m, purple), nanoeukaryotes (2-5 $\mu$m, black). Error bars represent standard deviations of the binned data over 100 km intervals.

Fig 4. Phytoplankton cellular growth rates across distance from the gyre boundary.

Phytoplankton cellular growth rates (d⁻¹) relative to distance (km) from the gyre boundary (grey bar), with negative distances indicating locations within the gyre and positive distances representing locations outside the gyre. Colored lines represent the cellular growth rates of different phytoplankton groups: Prochlorococcus (orange), Synechococcus (red), picoeukaryotes (<2 $\mu$m, purple), nanoeukaryotes (2-5 $\mu$m, black). Prochlorococcus abundance drops below detection during NSU1 and NSU2 outside the gyre. Error bars represent standard deviations of the binned data over 100 km intervals. Note that error bars are shown when the ship spent more than 24 hours within a 100 km interval.

Fig 5. Nutrient-phytoplankton relationships.

Correlation matrix between temperature, dissolved inorganic nitrogen (DIN) and dissolved inorganic phosphorus (DIP), cellular growth rate of Prochlorococcus, Synechococcus, picoeukaryotes (<2 $\mu$m), nanoeukaryotes (2-5 $\mu$m), and their biomass. Only correlations with statistical significance (p < 0.01, after Benjamini $\&$ Hochberg correction for multiple comparisons) are shown; positive correlations are in shades of red, negative correlations in blue, with color intensity indicating the strength of the Pearson correlation coefficient (r). White cells indicate non-significant correlations (p > 0.01). Sample size varied for different correlation pairs due to casewise deletion of missing values (n ranged from 73 to 132 observations, with a average of 118 observations per correlation pair).