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A Model for Methylmercury Uptake and Trophic Transfer by Marine Plankton Amina Traore Schartup, Asif Qureshi, Clifton Dassuncao, Colin Pike Thackray, Gareth Harding, and Elsie M. Sunderland Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b03821 • Publication Date (Web): 11 Dec 2017 Downloaded from http://pubs.acs.org on December 14, 2017
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Environmental Science & Technology
A Model for Methylmercury Uptake and Trophic Transfer by Marine Plankton Amina T. Schartup1,2,*, Asif Qureshi2,3, Clifton Dassuncao1,2, Colin P. Thackray1, Gareth Harding4, and Elsie M. Sunderland1,2 1
Harvard John A. Paulson School of Engineering & Applied Sciences, Harvard University, Cambridge, MA, USA 02138
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Department of Environmental Health, Harvard T. H. Chan School of Public Health, Harvard University, Boston, MA, USA 02214
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Department of Civil Engineering, IIT Hyderabad, Kandi, Sangareddy, TS 502285, India
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Bedford Institute of Oceanography, Dartmouth, NS, Canada
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Corresponding author: 29 Oxford Street, Cambridge, MA 02138;
[email protected] ACS Paragon Plus Environment
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Environmental Science & Technology
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Abstract
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Methylmercury (MeHg) concentrations can increase by up to 100,000 times between seawater
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and marine phytoplankton but levels vary across sites. To better understand how ecosystem
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properties affect variability in planktonic MeHg concentrations, we develop a model for MeHg
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uptake and trophic transfer at the base of marine food webs. The model successfully reproduces
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measured concentrations in phytoplankton and zooplankton across diverse sites from the
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Northwest Atlantic Ocean. Highest MeHg concentrations in phytoplankton are simulated under
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low dissolved organic carbon (DOC) and ultra-oligotrophic conditions typical of open ocean
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regions. This occurs because large organic complexes bound to MeHg inhibit cellular uptake and
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cell surface area to volume ratios are greatest under low productivity conditions. Modeled
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bioaccumulation factors for phytoplankton (102.4-105.9) are more variable than those for
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zooplankton (104.6-106.2) across ranges in DOC (40-500 µM) and productivities (ultra-
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oligotrophic to hyper-eutrophic) typically found in marine ecosystems. Zooplankton growth
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dilutes their MeHg body burden but they also consume greater quantities of MeHg enriched prey
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at larger sizes. These competing processes lead to lower variability in MeHg concentrations in
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zooplankton compared to phytoplankton. Even under hyper-eutrophic conditions, modeled
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growth dilution in marine zooplankton is insufficient to lower their MeHg concentrations,
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contrasting findings from freshwater ecosystems.
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Introduction
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wildlife and is the only form of mercury (Hg) that biomagnifies in food webs.1,2 Marine fish and
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shellfish account for more than 90% of the population-wide MeHg intake in the United States.3
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Concentrations of MeHg in phytoplankton can be up to 100,000 times higher than seawater.
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However, few studies have examined how ecosystem properties affect differences in MeHg
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uptake and trophic transfer at the base of marine food webs.4,5 Here, we develop a new model for
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MeHg bioaccumulation in marine phytoplankton and zooplankton.
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Methylmercury (MeHg) is a potent neurotoxin and oxidative stressor in humans and
Marine phytoplankton are thought to accumulate MeHg mainly by passive uptake from
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seawater (diffusion) across the cell membrane.6,7 Surface area to volume ratios of phytoplankton
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are therefore critical for anticipating total uptake.8 When ecosystems are less productive, smaller
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phytoplankton with greater surface area to volume ratios are more abundant to maximize nutrient
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uptake efficiency, which effectively increases MeHg uptake.9,5 Conversely, higher nutrient status
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can lead to a greater abundance of larger cells, reducing nutrient uptake at the base of the food
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web10 and potentially also MeHg uptake.
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Prior work suggests MeHg trophic transfer from phytoplankton to zooplankton is mainly
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driven by dietary intake with smaller direct uptake from seawater (10-20%).11 Loss pathways for
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MeHg in zooplankton include growth dilution and temperature dependent elimination in fecal
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pellets.11,12 Herbivorous (small) zooplankton grow most rapidly at higher temperatures and when
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sufficient nutrients are available.13 Omnivorous (large) zooplankton are opportunistic feeders and
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preferentially consume the largest prey available (other smaller zooplankton) but will also
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consume phytoplankton, depending on availability.14 Biomass dilution has been established as a
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major factor controlling MeHg concentrations in zooplankton from eutrophic freshwater
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systems.6,15 Similar processes for marine ecosystems have been hypothesized but not directly
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observed.4
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High concentrations of terrestrial dissolved organic matter may inhibit phytoplankton
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MeHg uptake by forming large complexes with MeHg in seawater that reduce transport across
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the cell membrane.16–19 By contrast, higher MeHg concentrations in marine zooplankton exposed
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to elevated dissolved organic matter concentrations were reported in mesocosm experiments by
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Jonsson et al.20 In these experiments, the algal community shifted from predominantly
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autotrophic (phytoplankton) to heterotrophic (bacterioplankton) at high dissolved organic matter
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concentrations. MeHg increases in zooplankton reflected lengthening of the food web rather than
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size based effects on phytoplankton community composition. This example illustrates why
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evaluating and diagnosing the role of simultaneously occurring factors that affect MeHg uptake
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and trophic transfer is essential for understanding differences in MeHg bioaccumulation across
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marine ecosystems.
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Here we use experimental data and bioenergetic theory to develop a model that links
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ecosystem properties to MeHg uptake in phytoplankton and trophic transfer to zooplankton.
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Field measurements from coastal, shelf and pelagic regions of the Northwest Atlantic Ocean are
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used to evaluate the model. We apply the model to quantitatively bound differences in MeHg
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accumulation attributable to variability in primary productivity, trophic structure, and dissolved
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organic carbon concentrations across ecosystems.
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Methods
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Model overview
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We develop a non-steady state model to calculate changes in MeHg concentrations in
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phytoplankton and zooplankton due to varying seawater MeHg concentrations and across
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different life stages for zooplankton. The model solves coupled first-order differential equations
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for zooplankton MeHg concentrations (wet weight) using one-step forward Euler-type numerical
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integration. Dissolved MeHg concentrations are used to force the simulation and can be specified
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deterministically or as distributions (probability density functions). Monitoring data are used to
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specify probability density functions for temperature, DOC and Chl a distributions in each
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ecosystem as input parameters that are simulated over 103 Monte Carlo iterations.
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Phytoplankton
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Our model includes three size classes of phytoplankton (picoplankton: 0.2-2 µm;
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nanoplankton: 2 – 20 µm, and microplankton: 20-200 µm. The relative abundance of different
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phytoplankton size classes is based on empirical relationships with surface (Chl a)
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concentrations (Supporting Information (SI), Table S1).9
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Phytoplankton MeHg concentrations are modeled using experimental net MeHg uptake
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rates from Lee and Fisher5 for several marine phytoplankton species. Concentrations reflect
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integrated uptake over 4 hours, after which the cells are assumed to achieve equilibrium.5 Lee
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and Fisher5 find no relationship between MeHg uptake rates and temperature and nutrients but a
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strong linear correlation between cell surface area (SA) to volume (V) ratios (Figure 1A; Table 1).
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We combine this information with data showing an exponential decline in uptake (R2 = 0.78)
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with increasing DOC concentrations from Luengen et al.17 (Figure 1B). The resulting expression
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for phytoplankton MeHg uptake rate (U) varies as a function of both cell-size and DOC
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concentrations in seawater (Table 1).
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Zooplankton
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We develop different model parameterizations for MeHg accumulation by herbivorous
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(small) and omnivorous (large) zooplankton based on established theory of growth and diet
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composition. For both, changes in MeHg concentrations (CZ, ng g-1) are based on first-order rates
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for: (1) seawater uptake (kB, d-1), (2) dietary intake from consumed prey (kD, d-1), (3) fecal
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elimination (kE, d-1), and (4) growth dilution (kG, d-1), as follows:
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= + − ( + ) ∙
[1]
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Direct uptake from seawater (bioconcentration) is based on the dissolved MeHg
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concentration in seawater and an octanol-water partition coefficient for methylmercuric chloride
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(SI Table S2). Dietary assimilation efficiencies for MeHg have been shown to range between
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50% and 70%11 and are simulated probabilistically using a uniform distribution. MeHg
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elimination by zooplankton is parameterized as a function of body burden and seawater
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temperature (SI Table S2). Ingestion rates for all zooplankton are based on energy needed for
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growth and metabolic function.21
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Growth is parameterized differently for herbivorous and omnivorous zooplankton.
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Herbivorous zooplankton growth is driven by temperature and surface productivity (Chl a)
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following the relationship developed for marine copepods by Hirst and Bunker (SI Table S2).13
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The composition of food consumed and associated dietary MeHg uptake is based on seawater
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filtration and the availability of different size classes of phytoplankton (SI Table S2).
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Omnivorous (large) zooplankton growth is based on standard bioenergetics that
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characterize energy requirements for growth (G, g d-1, Table S3). Energy obtained from prey
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consumption (I, g g-1 d-1, SI Tables S3 and S4) is allocated toward metabolism (respiration (R)
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and elimination (E), g g-1 d-1), and the difference is used to grow:
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=
= ( − − ) ∙
[3]
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where M is zooplankton (g) mass and t is time (d). Species-specific von Bertalanffy growth
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curves from the literature are used to constrain ingestion rates needed for growth.22 Omnivorous
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zooplankton graze primarily on herbivorous zooplankton and occasionally on large
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phytoplankton (microplankton).23 Diet composition is weighted toward the largest available prey
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that falls below a predator-prey length ratio constraint derived from other studies.24–26 Prey size
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consumed increases with length and gape size (SI Table S5).27 We assume omnivorous
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zooplankton will preferentially consume microplankton of comparable size to copepods (
