Diatom growth, biogenic silica production, and grazing losses to microzooplankton during spring in the northern Bering and Chukchi Seas
Introduction
While predicting future productivity in the Bering Sea (BS) and Chukchi Sea (CS) is important, a more pressing concern in this system is determining the fate of primary production within the food web. Existing data in the BS show that annual primary productivity is higher in years with poorer survivorship of age-0 walleye pollock (Theragra chalcogramma)―the most important regional and global (2014 data) fishery by landings (Eisner et al., 2014; FAO, 2016; Hunt et al., 2011). The lack of a significant correlation between fisheries potential and annual primary production could imply not-direct or non-linear relationships between these rates. Indeed, the 2019 Ecosystem Status report for the eastern BS show no correlation between the annual mean abundance of large copepods and euphausiids (age-0 walleye pollock prey) and the average primary production rate during the growing season, whereas there is a positive correlation between smaller copepods (not as favorable for age-0 walleye pollock) and primary production (Kimmel et al., 2019; Nielsen et al., 2019). Such a lack of understanding limits our predictive capability to determine whether hypothetical increases in future primary production may fuel enhanced higher trophic biomass in the pelagic or benthic realms. Whether diatoms will continue to have a dominant role in regional spring productivity is also unknown. Bottom-up factors, e.g. warming, could reduce diatoms’ element per unit biovolume (i.e. elemental density), and therefore reduce the quantity of carbon produced (Krause and Lomas, 2020; Lomas et al., 2019), even if other bottom-up factors (increased light, nutrient fluxes) favor faster growth rates. Understanding the fate of diatom primary production has important ramifications, from modeling changes in regional biogeochemical cycles to diagnosing whether the ecosystem will sustain economically important services.
While multiple groups of phytoplankton persist in the high-latitude Alaskan Seas, larger cells such as diatoms play key food-web roles, especially during blooms in both the spring and summer (Giesbrecht and Varela, 2021; Krause and Lomas, 2020; Yang et al., 2015). During the spring, the phytoplankton community increases biomass and fuels efficient transfer of energy and materials to higher trophic levels; under such conditions diatoms dominate phytoplankton biomass and the community rate of primary production (Baumann et al., 2014; Lomas et al., 2012). During cold-anomaly years in the eastern BS, Baumann et al. (2014) observed that diatom contribution to total phytoplankton biomass averaged 80% in the spring. A recent analysis of data from 2006 through 2016 demonstrated that warm anomaly years have higher phytoplankton biomass but the size structure is not significantly different from cool anomaly years (Lomas et al., 2020).
Microzooplankton (MZP) and larger mesozooplankton (LMZP e.g. calanoid copepods, euphausiids) are important consumers of regional phytoplankton productivity (Campbell et al., 2016; Sherr et al., 2013). Relative to most phytoplankton groups, diatoms’ larger size makes them favorable food sources for LMZP, which are themselves important prey items for age-0 class walleye pollock. On the eastern BS shelf, stable isotope data suggest LMZP graze more heavily on diatoms and other primary producers than MZP (Morales et al., 2014). However, analyses based on direct feeding experiments have shown that while LMZP prefer MZP as prey, in the spring and early summer, MZP biomass is minor compared to phytoplankton, and therefore, phytoplankton dominate LMZP diets under these conditions (Campbell et al., 2016). Such direct ingestion allows for a more efficient trophic transfer of phytoplankton organic matter than “phytoplankton → MZP → LMZP” pathways (Sherr et al., 2013; Stoecker et al., 2014a; Yang et al., 2015), which compound respiration losses from the increased number of trophic steps. Thus, processing primary productivity through the microbial loop may be one of the underlying factors affecting the observed spatial variations in organic matter quality based on C:N ratios, e.g. Grebmeier et al. (1988).
Regional studies show that MZP can be a major carbon pool within the food web for higher consumers (e.g. copepods) and they can consume significant quantities of primary production. Previous studies demonstrate that MZP biomass in these systems are variable and, at times, can exceed phytoplankton biomass by multiple factors, ranging from 0.2 to 109 μg C L−1 during spring (Sherr et al., 2013) and 1– >150 μg C L−1 during summer (Olson and Strom, 2002; Stoecker et al., 2014b; Strom and Fredrickson, 2008; Yang et al., 2015). Similarly, summer studies have observed that MZP carbon can exceed phytoplankton carbon, especially when chlorophyll a (Chl a) concentrations are low. During the Bering Ecosystem Study (BEST) and Bering Sea Integrated Ecosystem Research Program (BSIERP), it was recognized that there is a seasonal increase in the relative importance of MZP grazing relative to phytoplankton growth. In the spring, MZP grazing rates averaged 46% of phytoplankton growth among bloom and non-bloom conditions (Sherr et al., 2013). Farther north, in the CS and Beaufort Sea during late spring and early summer (Shelf–Basin Interactions program), Sherr et al. (2009) observed that MZP grazing consumed between 0 and 120% of daily primary production (note: >100% losses of daily primary production reduces phytoplankton standing stock), with an average of 22% ―approximately half the spring rates observed during BEST/BSIERP. More recent results demonstrated similar variability in the CS during spring 2014, where MZP grazed 31–>100% of primary production, with an average of 46% (Connell et al., 2018). While these data demonstrate that MZP can be an important control on total phytoplankton biomass and productivity, size-fractionated data for the BS are only reported for the summer (Olson and Strom, 2002; Strom and Fredrickson, 2008). During summer in the Chukchi, Yang et al. (2015) directly quantified diatom losses to MZP (based on cell counts), and showed it was substantial (63% ± 21% SD of diatom production); however, whether this is similar in the spring is unknown. The lack of size-fractionated data during spring precludes us from understanding which phytoplankton size classes are being controlled by MZP. Sherr et al. (2013) note that the disparity in growth rates between MZP and diatoms during early bloom stages in the BS is due to the lag of MZP growth rate to availability of phytoplankton prey (i.e. MZP growth approaches maximum rates at high prey biomass levels). This disparity during spring suggests that regional diatoms could grow (at times) with minor losses due to MZP. Such a condition would enable a high proportion of diatom carbon being directly consumed by higher trophic level organisms (e.g. LMZP, larval fish) and/or exported to the benthos via sedimentation (e.g. single cell sinking, association with aggregates).
In this study, we report rates of diatom growth and productivity, along with rates for MZP grazing on both large (≥5 μm) and small (<5 μm) phytoplankton during spring in the northern BS and CS during a year experiencing early-ice retreat and anomalously warm temperatures (Baker et al., 2020; Walsh et al., 2018). The grazing measurements are coupled to measurements of diatom productivity using a silicon tracer method, as diatoms are the only major phytoplankton group having an obligate silicon requirement. Such early-ice retreat conditions may affect regional food web phenology by altering when the main phytoplankton bloom occurs and the growth/success of consumers which require this production pulse. Given the projected warming trends through the end of the 21st century for the pan-Arctic region (IPCC, 2014) and the potential for ecological reordering in this region (Huntington et al., 2020), understanding the proportion of primary production which is consumed by MZP will be important for setting upper limits for the availability of primary production to higher trophic organisms in this system.
Section snippets
Collection and hydrography
Microzooplankton grazing, phytoplankton growth, and diatom productivity rates were measured during the Arctic Shelf Growth, Advection, Respiration and Deposition (ASGARD, Chief Scientist S. Danielson) cruise in the northern BS and CS aboard the R/V Sikuliaq from 9 – 28 June 2017 (Fig. 1). Hydrographic properties were measured using a SeaBird SBE CTD equipped with a Biospherical QSP-240 photosynthetically active radiation (PAR) meter, Wetlabs FLRTD fluorometer and SeaBird SBE 43 O2 meter. Water
Hydrography and nutrients
The general climatology during ASGARD 2017 was warm relative to average conditions (Danielson et al., 2020; Huntington et al., 2020). Generally, the progression of sea-ice retreat was consistent from south to north based on data within three subareas in the southeastern BS, northern BS, and the CS (Fig. 1). An oscillation between warm and cold intervals between 2000 and 2019 for a small area in the southeastern BS (Fig. 1B) alters the ice retreat timing by plus or minus one month compared to
Bottom-up regulation of phytoplankton growth rates
Dilution experiments enable an assessment of both bottom-up and top-down factors concurrently. The caveat for comparing phytoplankton growth rates to bottom-up factors is that dilution experiments must successfully conform to the methodological assumptions (Landry and Hassett, 1982). Non-zero rates for the small-phytoplankton size class were quantified in 70% of our experiments, twice the number of experiments where non-zero rates were quantified for large phytoplankton. A correlation analysis
Author contributions
JWK and MWL conceived of the study which was enabled by collaboration with SLD. All authors collected samples and provided original data from the ASGARD cruise (led by SLD). Data analysis was led by JWK and MWL. All authors contributed to the writing the manuscript.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
Funding was provided by the National Science Foundation Office of Polar Programs (OCE-1603605, JWK; OCE-1603460; MWL), logistic and vessel support by the North Pacific Research Board (A91-99a and A91-00a to SLD; NA15NMF4720173 to MWL, subaward to JWK), and vessel support from the Alaska Sikuliaq Program (SLD). We thank the ASGARD cruise (SKQ201708T, SKQ201709S) science party and crew including marine technicians S. Hartz, E. Roth; S. Baer, L. Eisner, D. Wiik, T. Martinson, and D. Harlan for
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