Revealing biotic and abiotic controls of harmful algal blooms in a

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Revealing biotic and abiotic controls of harmful algal blooms in a shallow subtropical lake through statistical machine learning Natalie Genevieve Nelson, Rafael Muñoz-Carpena, Edward J. Phlips, David Kaplan, Peter Sucsy, and J. Hendrickson Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.7b05884 • Publication Date (Web): 24 Feb 2018 Downloaded from http://pubs.acs.org on February 25, 2018

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Environmental Science & Technology

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TITLE

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Revealing biotic and abiotic controls of harmful algal blooms in a shallow subtropical

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lake through statistical machine learning

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AUTHORS

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Natalie G. Nelson1,2, Rafael Muñoz-Carpena1*, Edward J. Phlips3, David Kaplan4, Peter

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Sucsy5, John Hendrickson5

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AUTHOR AFFILIATIONS

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Florida, Gainesville, FL, USA

Hydrology & Water Quality, Agricultural & Biological Engineering, University of

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Raleigh, NC, USA

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of Florida, Gainesville, FL, USA

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Engineering Sciences Department, University of Florida, Gainesville, FL, USA

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* corresponding author: [email protected]

At present: Biological & Agricultural Engineering, North Carolina State University,

Fisheries & Aquatic Sciences, School of Forest Resources & Conservation, University

Engineering School of Sustainable Infrastructure and Environment, Environmental

St. Johns River Water Management District, Palatka, FL, USA

ACS Paragon Plus Environment

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ABSTRACT

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Harmful algal blooms are a growing human and environmental health hazard globally.

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Eco-physiological diversity of the cyanobacteria genera that make up these blooms

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creates challenges for water managers tasked with controlling the intensity and frequency

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of blooms, particularly of harmful taxa (e.g., toxin producers, N2 fixers). Compounding

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these challenges is the ongoing debate over the efficacy of nutrient management

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strategies (phosphorus-only versus nitrogen and phosphorus), which increases decision-

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making uncertainty. To help improve our understanding of how different cyanobacteria

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respond to nutrient levels and other biophysical factors, we analyzed a unique 17-year

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dataset comprising monthly observations of cyanobacteria genera and zooplankton

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abundances, water quality, and flow a bloom-impacted, subtropical, flow-through lake in

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Florida (USA). Using the Random Forests machine learning algorithm, an assumption-

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free ensemble modeling approach, we characterized and quantified relationships among

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environmental conditions and five dominant cyanobacteria genera. Results highlighted

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nonlinear relationships and critical thresholds between cyanobacteria genera and

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environmental covariates, the potential for hydrology and temperature to limit the

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efficacy of cyanobacteria bloom management actions, and the importance of a dual

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nutrient management strategy for reducing bloom risk in the long-term.

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INTRODUCTION Increases in the frequency, magnitude, duration, and geographic range of harmful

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cyanobacterial blooms related to cultural eutrophication and climate change (1–3) have

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raised concerns about undesirable future changes in the structure and function of

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freshwater ecosystems (4–8). Of particular concern are cyanobacteria species that

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threaten ecological and public health through the production of toxins, formation of

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scums that shade out benthic primary producers, and excess accumulation of biomass that

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can result in hypoxia (9).

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Although cyanobacteria are found in most aquatic environments, their blooms are

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particularly widespread and intense in eutrophic freshwater systems (9). The ubiquity of

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cyanobacteria is attributable to a diversity of physiological adaptations that allow them to

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successfully compete for limited resources in a wide range of habitat types (1,2,10). Such

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adaptations include N2 fixation (11,12), luxury nitrogen (N) and phosphorus (P) uptake

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(10,13), buoyancy regulation using gas vesicles (14), sustained growth at elevated

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temperatures (7), and grazer avoidance (15,16), among others.

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Considering the eco-physiological diversity exhibited by cyanobacteria taxa offers

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insight into how cyanobacteria outcompete other phytoplankton, but it does not

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necessarily help clarify the factors that drive the dynamics of cyanobacteria populations

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and formation of bloom events in individual ecosystems (17,18). This issue is central to

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challenges faced by water managers who are tasked with developing appropriate actions

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for not only controlling the intensity and frequency of blooms, but also reducing the

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potential for blooms of harmful taxa (e.g., toxin producers). These challenges are further

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compounded by an ongoing debate regarding the efficacy of P-only (“single nutrient”)


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versus N-and-P (“dual nutrient”) management strategies for cyanobacteria bloom

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abatement in aquatic ecosystems (19–23).

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The primary goal of this study was to address the growing need for increased

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understanding of the environmental conditions that control blooms of important

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cyanobacteria genera and to inform water managers’ adoption of nutrient management

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strategies for bloom mitigation. Our specific objectives were to: (1) quantify and

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characterize taxa-specific relationships between cyanobacteria biomass and

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environmental conditions; and (2) evaluate the efficacy of nutrient management strategies

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relative to several important cyanobacteria taxa. To do so, we applied the Random

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Forests method, an assumption-free, ensemble-modeling machine learning approach, to a

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long-term (17-year) dataset composed of monthly observations of physical and chemical

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parameters, flow, and biomass of cyanobacteria and zooplankton taxa in Lake George, a

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subtropical flow-through lake of the iconic St. Johns River (Florida). To our knowledge,

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this is the first investigation to concurrently characterize relationships between bloom-

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forming cyanobacteria genera and biological, chemical, and physical covariates, as well

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as to apply the Random Forests methodology to the assessment of cyanobacteria

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dynamics. Results offer new insights into how diverse cyanobacterial assemblages

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respond to top-down and bottom-up controls over a long-term record, offering insights

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that are broadly applicable to other freshwater systems.

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METHODS Site description – The St. Johns River is a subtropical blackwater system that drains 24,424 km2 of Florida’s northeastern region (USA) (24). The St. Johns flows from


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south to north through approximately 500 km of meandering river reaches and flow-

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through lakes before discharging into the Atlantic Ocean (Figure S1). The largest of these

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flow-through lakes is Lake George (18,934 ha), a shallow system (mean depth of 3 m)

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located approximately 210 km upstream from the mouth of the river (25). Hydrologic

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inputs to Lake George include the St. Johns River (78.9% of the lake’s volume), rainfall

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(8.7%), flow from artesian springs (8.3%), and runoff (4.1%) (25). Turnover times in the

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lake are estimated to range from 24 to 180 days depending on flow conditions (26). Lake

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George’s waters are amber in color due to the presence of high levels of colored

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dissolved organic matter, concentrations of which peak from fall to early spring (24).

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Lake George is eutrophic (TP concentrations range from approximately 30-160

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µg L-1) and affected by recurrent and severe cyanobacteria blooms (24,27). In terms of

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carbon biomass, cyanobacteria account for over 90% of the total phytoplankton observed

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in this system. Cyanobacteria in Lake George display distinct seasonal patterns that

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diverge from traditional spring-summer-fall-winter variation. Instead, cyanobacteria

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periodicity in this subtropical, flow-through setting is better explained by “cold” (January

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– April), “warm” (May – August), and “flushing” (September – December) seasons

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(27,28). On average, cyanobacteria carbon biomass in Lake George is greatest in the

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warm season, followed by the flushing season (27). Dataset – Data evaluated in this study included monthly water quality

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observations, phytoplankton and zooplankton species counts, and flow rates from

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October 1993 to December 2010. Data were collected at a long-term monitoring site

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(LG1.2, see Figure S1a) located at the outlet of Lake George. Phytoplankton and

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zooplankton species identifications and enumerations were done using inverted light


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microscopes according to methods described by Srifa et al. (27). Water quality

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parameters associated with the collection of water for plankton counts were obtained

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from the St. Johns River Water Management District. Regularly-measured constituents

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included alkalinity, chlorophyll, chloride, color, conductivity, dissolved oxygen, pH,

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pheophytin, Secchi depth, sulfate, total dissolved and suspended solids, total organic

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carbon, turbidity, water temperature, dissolved ammonium, dissolved phosphate, total

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phosphorus (TP), and total Kjeldahl nitrogen (TKN). Light extinction due to tripton

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(Ktripton, m-1) was predicted from the chlorophyll-a, color, and Secchi depth data

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(Equation S1).

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Zooplankton and cyanobacteria biovolumes were transformed into carbon

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biomass (mg C L-1) using a carbon conversion factors of 0.075 and 0.22 pg C µm-3,

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respectively (29,30). Daily flow data were collected in the St. Johns River by the U.S.

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Geological Survey (USGS) at site 02236000 in Deland, FL (“flow monitoring” site in

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Figure S1a). The USGS maintains a flow monitoring site nearer the inlet to Lake George

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(site 02236125 in Astor, FL), but these data included several gaps over the study period.

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Flow data collected at the Deland and Astor sites were compared to ensure that the

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Deland data were representative of Lake George’s inflow dynamics (Figure S2); the data

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were related by a Pearson’s correlation coefficient of 0.96 and a Nash-Sutcliffe

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Efficiency (Equation S1) of 0.915, leading us to conclude that the use of Deland data was

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acceptable for this analysis. Data processing details are provided in the Supporting

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Information.

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Random Forests modeling – We utilized Random Forest models to quantify and

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characterize taxa-specific cyanobacteria-environmental relationships. Random Forests is


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a machine learning algorithm used to fit a large ensemble (or, “forest”) of randomly-

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assembled de-correlated classification (discrete data) or regression (continuous data) trees

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to bootstrapped samples of a response variable, and the outputs of these trees are

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averaged to produce a simulated response (31–33). The Random Forests modeling

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framework was selected for this analysis because of its abilities to (1) handle data

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produced from complex interactions (33) and (2) uncover nonlinear and linear

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relationship structures (32,34), making this approach ideal for uncovering the functions

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relating cyanobacteria genera to environmental and trophic covariates.

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While Random Forests models are often viewed as “black boxes,” methods exist

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for quantifying how these statistically derived models relate input explanatory variables

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to produce simulated responses. Such measures include permutation importance, partial

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dependence, and relative sensitivity. Permutation importance describes the change in

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Mean Squared Error (MSE) that occurs when a fitted model is run with a randomly

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permuted explanatory variable (34,35). Partial dependence is a measure of an explanatory

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variable’s influence on the response variable given the effects of all other explanatory

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variables in the model (33,34), and is calculated across the range of each explanatory

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variable’s observations. Relative sensitivity is calculated from the partial dependence

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curves to summarize the ranges over which partial dependencies varied relative to

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changes in the explanatory variables; if partial dependence greatly varies over a narrow

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range of an explanatory variable (i.e., the partial dependence curve has a steep slope),

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then the response variable is said to have a high relative sensitivity to that explanatory

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variable.


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Models were fit and tested through 5-fold cross validation (33), which was

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performed using the following steps: (1) partition dataset into training and testing folds,

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(2) “grow” Random Forests, (3) quantify model performance using the Nash-Sutcliffe

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Efficiency, (4) tabulate permutation importance, partial dependence, and relative

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sensitivity of all the explanatory variables, and (5) repeat steps (2)-(4) 4 times, with each

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new fold representing the “testing” set on each iteration. This modeling framework was

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repeated 5 times for each response variable to evaluate variability in model outputs; thus

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a total of 25 random forest models were produced with each application (5 repetitions of

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each 5-fold cross validation). Details associated with each of these steps are provided in

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the Supporting Information.

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Response and explanatory variables – The dominant cyanobacteria genera –

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defined here as genera that accounted for 5% or greater of the total cyanobacteria carbon

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biomass (mg C L-1) over the study period – were designated as the response variables in

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the random forests modeling analysis.

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TKN (mg L-1), TP (mg L-1), dissolved NH4 (mg L-1), dissolved PO4 (mg L-1),

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water temperature (°C), average flow (m3 s-1), partial light extinction due to tripton

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(Ktripton, m-1), color (CPU), copepods (mg C L-1), and rotifers (mg C L-1) were included as

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explanatory variables in the Random Forest models. Ktripton was calculated from Secchi

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depth, chlorophyll-a, and color (see Supporting Information). This reduced set of

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factors was selected based on reported relationships between these covariates and

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cyanobacteria (2,25,27,36–38). Excluded variables are outlined in the Supporting

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Information, along with justification for their exclusion. All explanatory variables were


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lagged by one time step (1 month) to reflect the division rates of cyanobacteria in natural

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environments (13,39).

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RESULTS Summary of observations – The Anabaena (N2 fixers), Cylindrospermopsis (N2

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fixers), Planktolyngbya (non-fixers), Microcystis (non-fixers), and Oscillatoria (non-

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fixers) groups dominated the Lake George cyanobacteria community over the study

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period (Table S1). It is important to note that the Oscillatoria group includes several

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genera (e.g., Planktothrix and Limnothrix) that were further divided from Oscillatoria

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and renamed during the data collection period (40); similarly, the Anabaena group

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includes members of the genus recently renamed to Dolichospernum (41). Given that

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these changes occurred well into the study period, we have reported these groups per the

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prior nomenclature since observations were recorded in context of these broader

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classifications.

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Cyanobacteria biomass displayed strong inter-annual (Figure S3) and seasonal

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variability (Figure S4) across the dominant genera. Of the dominant genera, Oscillatoria

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produced the greatest total biomass over the study period, and Anabaena the least (Table

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S1). Interestingly, Microcystis regularly bloomed prior to 2001, and minimally varied at

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low biovolumes thereafter (Figure S3). Cyanobacteria predominantly flourished in the

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warm season, followed by the flushing season (Figure S4); Anabaena typically bloomed

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prior to the other genera on a seasonal basis (Figure S4). Additional description of the

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observed data is included in the Supporting Information.


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Model performance – Models fit the training data well, as measured by Nash

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Sutcliffe Efficiency (NSE) across the 25 model applications per response variable (Figure

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1a); the minimum NSE value was 0.77 (an Anabaena model) and the max was 0.91 (a

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Planktolyngbya model). Previous studies have proposed that models with NSE > 0.65 are

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“acceptable” (42), indicating that all the training Random Forest models presented here

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satisfactorily simulated cyanobacteria genera dynamics. However, models did not

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perform as well when predicting the testing data (Figure 1b). Specifically, the model

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suites included efficiencies below 0 when evaluated against the testing data, which

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suggests that findings reported here were not generalizable across the entire study period;

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rather, marked effects of particular relationships were important for subsets of the period

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of record.

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Permutation importance – Color and water temperature were associated with

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the greatest permutation importance (quantified through percent change in MSE) in the

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Cylindrospermopsis (Figure 2b), Planktolyngbya (Figure 2c), and Oscillatoria (Figure

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2e) models; these explanatory variables were also among the most important in the

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Anabaena (Figure 2a) and Microcystis (Figure 2d) models. Overall, permutation of

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explanatory variables did not dramatically change the percent MSE in any of the models.

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However, water temperature appeared to be a particularly influential variable in the

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Planktolyngbya model (Figure 2c). As the Planktolyngbya model suite had the highest

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testing NSE results, the variable importance results suggest that permuted importance

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also served as a predictor of model testing success.

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Partial dependence – Plots of partial dependence revealed predominantly nonlinear model relationships between the lagged explanatory variables and


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cyanobacteria genera (Figure 3). Partial dependence curves correspond to the

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relationships linking response and explanatory variables, and the curves are comprised of

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the average modeled values (in units of the response variable) across the range of

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explanatory variable observations. The steepest curves were associated with TKN, TP,

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average flow, color, water temperature, and copepod abundance, whereas the curves for

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NH4, PO4, Ktripton, and rotifer abundance curves were largely invariant.

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Non-fixing cyanobacteria genera (Planktolyngbya, Microcystis, and Oscillatoria)

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displayed a relatively strong partial dependence on TKN (Figure 3a). Specifically, these

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curves depict a threshold in the relationship between TKN and non-fixers where partial

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dependence rose sharply TKN concentrations between 1.5-2.5 mg L-1, but plateaued in

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the range of 2.5-3 mg L-1. Note, however, that there were few observations at high TKN

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concentrations, limiting interpretation in this range. Anabaena and Cylindrospermopsis

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showed little partial dependence on TKN; however, these partial dependence curves

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revealed a slight sensitivity of N2 fixers to TKN at low TKN concentrations.

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The cyanobacteria genera largely lacked partial dependence on TP, with

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Microcystis being an exception (Figure 3b). Microcystis’ partial dependence on TP

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indicated a sensitivity to TP at low concentrations (decreasing carbon biomass with

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increasing TP) up until a concentration approximately 0.1 mg L-1, above which there was

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no additional dependence (i.e., similar to the “threshold” response described above).

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Average flow, color, and water temperature emerged as explanatory variables on

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which all of the cyanobacteria genera displayed notable partial dependence (Figure 3e).

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Specifically, cyanobacteria were more abundant at low flows and colors, and higher

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temperatures. Although the color partial dependence curves were essentially identical


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across all cyanobacteria genera except Anabaena (Figure 3f), which peaked at

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approximately 120 CPU.

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Relative sensitivity – Relative sensitivities were calculated based on the median

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scaled partial dependence curves (Figure 4). The cyanobacteria genera were, on average,

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most sensitive to the physical covariates, followed by nutrient concentrations, then

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zooplankton abundance (average relative sensitivities to physical factors, nutrients, and

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zooplankton across all genera equaled 1.29, 0.45, and 0.41, respectively). Planktolyngbya

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(Figure 4c) and Oscillatoria (Figure 4e) were most sensitive to changes in water

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temperature, Anabaena (Figure 4a) and Microcystis (Figure 4d) were most sensitive to

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changes in average flow, and Cylindrospermopsis (Figure 4b) was most sensitive to water

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color. With regards to nutrients, the genera were generally more sensitive to TKN than

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TP, though Microcystis was similarly sensitive to TKN and TP (Figure 4d).

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DISCUSSION Historically, a number of researchers have argued that nutrient management is the

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most effective strategy for preventing cyanobacteria blooms regardless of the dominant

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taxa involved (17,43,44). While the results of this study provide some support for the

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potential efficacy of nutrient reduction strategies, certain aspects of the results highlight

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how nutrients alone do not always adequately explain trends in biomass of certain

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cyanobacteria taxa of particular concern from a management perspective (e.g. harmful

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algal bloom species). The importance of the latter caveat is illustrated by the relative

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sensitivity of different cyanobacteria genera to the range of explanatory variables

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included in this modeling effort. Overall, the genera were relatively more sensitive to


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TKN, TP, average flow, color, and copepod abundance. Because the genera were found

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to be largely insensitive to changes in NH4, PO4, light extinction due to tripton, and

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rotifer abundance, these covariates were excluded from the ensuing discussion.

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Sensitivity of Cyanobacterial Biomass to Nitrogen and Phosphorus Levels

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N2 fixing cyanobacteria were relatively insensitive to TKN (Figure 2a) due to

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their ability to utilize N2 as a nitrogen source for growth (13). In contrast, non-fixing

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genera showed increasing partial dependence on TKN with increasing concentrations

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until a threshold of 1.5-2.5 mg L-1 (Figure 3a, 2a). This finding indicates that

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management actions seeking to reduce TKN may produce observable decreases in non-

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fixer cyanobacteria biomass when this concentration threshold is crossed. The sharpest

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thresholding behavior was associated with Microcystis, which reflects the observation

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that after 2001 no major Microcystis blooms were observed in Lake George (Figure S3).

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The post-2001 period was also characterized by lower baseline and peak levels of TKN.

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It is possible that the relatively strong reliance of Microcystis on external nitrogen made it

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less competitive during the post-2001 period, as observed in some other ecosystems (45–

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47).

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Most cyanobacteria genera were less sensitive to changes in TP concentrations

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than to TKN, as demonstrated by the flatter TP partial dependence curves (Figure 3b).

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The somewhat elevated dependence of Microcystis biomass on the lower end of the TP

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concentration scale may reflect how elevated biomass levels generally appeared in mid-

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late summer when TP levels in the water column were often lower than in spring or early

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summer (Figure 3d). Microcystis aeruginosa is well known to have strong buoyancy

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regulation capacity (13,48). It is possible that during mid-summer, when average wind


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mixing energy is lower than in the spring, M. aeruginosa takes advantage of benthic

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fluxes of bioavailable phosphorus, which are enhanced by lower oxygen levels near the

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bottom of the water column (49,50), particularly under high summer water temperatures.

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The ability of buoyancy-regulating cyanobacteria to take advantage of elevated nutrient

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levels in different layers of the water column has been observed in other ecosystems (51).

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In more general terms, many of the major bloom-forming cyanobacteria species in Lake

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George are known to have differing degrees of buoyancy regulation (52), which may

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contribute to the apparent low sensitivity to TP levels, since sediment phosphorus

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reserves can serve as sources of nutrients somewhat independent of water column

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concentrations (51).

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Implications for Nutrient-Based Cyanobacteria Bloom Mitigation

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The cyanobacteria-nutrient relationships identified here provide some insight into

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the ongoing discussions in the literature of two nutrient management approaches:

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phosphorus only (19,20) versus dual control of both nitrogen and phosphorus (21–23).

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Although our results are from a single, shallow, subtropical lake, they highlight nuances

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that are broadly applicable when weighing the potential efficacy of these two approaches.

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The insensitivity of the cyanobacteria groups’ biomass to the range of TP values

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observed in Lake George raises questions about whether phosphorus reduction alone will

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significantly reduce intensities of certain types of cyanobacteria blooms. While the results

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of recent nutrient enrichment bioassay experiments in Lake George identified

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phosphorus- and phosphorus/nitrogen co-limited conditions for phytoplankton growth,

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these conclusions were produced from data collected during an extreme drought in 2000,

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when TP concentrations were very low (e.g., near 30 µg L-1) (25). Additionally, the


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modest sensitivity of N2 fixing species biomass to TP values below 0.06 µg L-1 observed

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in the Random Forests results, provides some limited evidence for the potential control of

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this functional group, possibly related to the relatively high demand some nitrogen fixers

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have for phosphorus (53,54). Recent mechanistic modeling efforts by the St. Johns River

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Water Management District identified an annual mean threshold of 0.05-0.063 mg TP L-1

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as a long-term target that would be effective for mitigating blooms (50). The differences

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between the findings of these prior studies and those presented here are challenging to

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reconcile, but could be explained by the aforementioned influences of internal loads from

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sediments and water column cycling of nutrients, as observed in some ecosystems (51).

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The range of results among this and other studies on cyanobacteria-phosphorus

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relationships in Lake George warrant further examination, focusing on the feasibility of

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reducing phosphorus levels within the context of both internal and external phosphorus

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sources.

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In contrast, the sensitivity of non-N2 fixing cyanobacteria to TKN (Figure 2a)

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suggests that significant reductions in nitrogen load do have the potential to reduce bloom

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intensities of those genera, though N2-fixing cyanobacteria are unlikely to be affected.

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Combined with those of TP, these TKN results suggest that the potential exists for

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control of N2 fixers through phosphorus reductions, and non-fixers through nitrogen

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reductions. However, other studies have shown that N2 fixation in many lakes may

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represent less than 50% of the N2 fixer nitrogen demand (55–57); therefore, these

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modeling results should be interpreted in the context of other experimental findings.

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The value of considering nitrogen load reduction in part depends on the specific management priorities for Lake George. For example, toxic blooms of the non-N2 fixing


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cyanobacterium Microcystis aeruginosa are a recurring problem for Lake George and the

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downstream portions of the lower St. Johns River (58). The negative response of

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Microcystis and other non-N2 fixing cyanobacterial biomass to TKN concentrations

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below 1.5 mg L-1 (Figure 3a) suggests that significant reductions in external nitrogen

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loads may contribute to less intense blooms of these groups. However, this conclusion

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may be in part dependent on the response of the N2 fixing cyanobacteria to reduced

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nitrogen loads. Currently, the N2 fixers Anabaena (most prominently the renamed genus

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Dolichospermum) and Cylindrospermopsis are major contributors to the nitrogen budget

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of Lake George (59).

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The latter observation raises two important considerations related to possible

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consequences of nitrogen reduction strategies: (1) the relative importance of Anabaena

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and Cylindrospermopsis biomass may increase relative to non-fixers and result in

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alternative challenges to the ecosystem, and (2) increases in N2 fixer biomass may lead to

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increases in nitrogen loads via N2 fixation to the system, which could ultimately fuel non-

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fixer blooms, particularly downstream of the lake. These considerations, and those

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associated with phosphorus reduction scenarios, argue for exploration of a dual

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phosphorus and nitrogen management strategy. The potential feasibility or efficacy of

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such an approach in other lakes more generally depends on the specific structure of

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individual ecosystems and the character of their external and internal sources of nutrient

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load.

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Sensitivity of Cyanobacterial Biomass to Other Abiotic and Biotic Variables

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Beyond nutrient-based management strategies, our study also identified important connections among cyanobacteria and other abiotic and biotic factors, which help to put


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the nutrient response observations into a more holistic management context. One of the

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challenges facing water managers is that many of these factors (e.g., water temperature,

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flow, color) are largely uncontrollable in the short-term, even though human activities

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will likely have strong impacts on them in future decades and centuries, such as changes

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in temperature, rainfall (e.g. as it relates to watershed inputs) and hydrologic conditions

361

(e.g. sea level rise, lake stage). For example, the strong positive relationship between

362

cyanobacteria biomass and temperature also corroborates the hypotheses of a number of

363

researchers that anticipated future global temperature increases will selectively favor

364

cyanobacteria (4,7,60).

365

It is also important to examine potential interactive effects among abiotic

366

explanatory variables to further define the extent to which nutrients influence

367

cyanobacteria dynamics, particularly when certain nutrients are not present in limiting

368

concentrations (17,61–63), as appears to be the case for phosphorus in Lake George.

369

High flow conditions in the fall and winter not only lead to reduced water residence times

370

and reduced light transmission due to elevated color levels, but occur during the period of

371

lowest incident light flux and water temperatures, all of which help to explain the low

372

potential for blooms of phytoplankton in general, despite the fact that it is also the period

373

of highest nutrient concentrations (24,27,36). The importance of these relationships is

374

reflected in the strong negative correlations between cyanobacterial biomass and both

375

flow and color.

376

Previous studies of Lake George have highlighted how hydrologic conditions can

377

override or exaggerate the effects of other environmental factors, such as nutrient levels,

378

on cyanobacteria dynamics (27), corroborating the results presented here. Understanding


17


Page 18 of 35

379

the degree to which the hydrologic regime decouples cyanobacteria from nutrient

380

dynamics is critical to understanding the potential efficacy of water quality management

381

practices. We caution, however, that there are substantial physical and/or fiscal barriers

382

associated with changing a system’s hydrology. Unless managers have the capacity to store

383

and release large amounts of freshwater, their ability to control bloom potentials is likely limited

384

to nutrient management. Therefore, it is ultimately the “nutrient knob” (64) that provides the most

385

reliable management strategy for long-term bloom mitigation (43,44,64).

386

Another consideration for defining the dynamics of cyanobacteria populations is

387

the role of top-down controls, both in terms of direct grazing pressure and indirect trophic

388

cascade effects. The data available for the two dominant groups of zooplankton in Lake

389

George, rotifers and copepods, provide some insight into top-down effects. Non-N2 fixing

390

cyanobacteria had a positive near linear relationship with rotifer biomass, suggesting that

391

rotifers respond positively to increases in cyanobacteria, but do not appear to be able to

392

suppress bloom formation, as indicated by the lack of depression of cyanobacteria

393

biomass even at the highest abundances of rotifers (Figure 3j). The relative resistance of

394

many cyanobacteria to strong top-down control by zooplankton grazers has been widely

395

discussed in the literature, as it relates to the presence of grazing inhibitors (2,15,16), or

396

secondary trophic effects (60,65).

397

For copepods, the relationships to cyanobacteria were positive but non-linear,

398

with a narrow threshold range of response (Figure 3i). Interpreting the implications of

399

this relationship is complicated by the diverse trophic character of copepods, which

400

include many carnivorous, as well as, omnivorous taxa (66). The sharp response

401

threshold for the cyanobacteria-copepod relationship may in part reflect the seasonal

402

coincidence of peaks in copepod and cyanobacteria biomass. In addition, top-down


18

Page 19 of 35


403

pressure by copepods on smaller zooplankton grazers of phytoplankton (e.g. protozoans,

404

rotifers) may lower grazing pressure on cyanobacteria.

405

Methodological Implications

406

Ideally, mechanistic water quality modeling would effectively simulate time-

407

varying dynamics of cyanobacteria remains, however the capacity of such models

408

remains limited (67,68). At present, data-intensive, assumption-free methods (e.g.,

409

Random Forests models) are among the most rigorous tools available for the study of

410

complex organism community dynamics using long-term monitoring data. The Random

411

Forests machine learning algorithm utilized here offers a straightforward and assumption-

412

free approach to developing an initial appraisal of how important potentially manageable

413

(e.g., nutrient loads) versus non-manageable (e.g., water temperature) system features are

414

as predictors of cyanobacteria dynamics.

415

Although the Random Forests models were employed for explanatory modeling

416

(i.e., describing observed dynamics) in the case presented here, the use of 5-repeated 5-

417

fold cross validation provided insight into the degree to which the models could be used

418

for general prediction purposes. All of the model suites performed reasonably well when

419

applied to testing data (Figure 1b), which suggests that the explanatory variables

420

considered in this analysis are important descriptors of cyanobacteria dynamics.

421

However, some efficiencies associated with individual testing model runs were low (i.e.,

422

NSE < 0), which suggests that additional descriptors should be incorporated into the

423

models to increase their predictive capacities. Future research efforts should consider

424

evaluating whether cyanobacteria genera, as opposed to environmental covariates, better

425

predict the dynamics of other genera. Moreover, as this study was limited by the temporal


19


Page 20 of 35

426

resolution of the long-term monitoring data program, opportunities exist to expand this

427

analysis by repeating it in a setting with higher resolution data; given higher resolution

428

data, the robustness of the sensitivities and nonlinearities reported here could be assessed

429

across a variety of temporal scales.

430

Applying Random Forests models to a broad variety of aquatic systems impacted

431

by cyanobacteria blooms would help to advance our understanding of the factors that can

432

be managed to mitigate blooms, and such applications should be the focus of future

433

studies. This analysis serves as a case study to guide other researchers and practitioners in

434

their efforts to leverage machine learning tools for the study of water quality phenomena.

435 436 437

ACKNOWLEDGEMENTS This material is based upon work supported by the National Science Foundation

438

Graduate Research Fellowship under Grant No. DGE-0802270, USDA NIFA Hatch

439

Project 1011481, and St. John River Water Management District Contract No. 28650.

440

RMC acknowledgers support for the UF Water Institute Fellowship. The authors declare

441

that there are no conflicts of interest.

442 443

SUPPORTING INFORMATION

444

Document containing additional details on data processing, modeling workflow, and

445

summary of observed data.

446


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Page 21 of 35


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Sarnelle, O. Herbivore Effects on Phytoplankton Succession in a Eutrophic Lake.

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FIGURE CAPTIONS

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Figure 1. Nash-Sutcliffe Efficiencies (NSE) of the genera models when tested against (a)

646

training, and (b) testing data subsets. Each boxplot contains n=25 values corresponding to

647

the 5-repeated 5-fold cross-validation performed for each Random Forests model; each

648

value is shown as a green point.

649 650

Figure 2. Permuted importance of explanatory variables. X-axes are in units of % change

651

in Mean Squared Error. Each boxplot includes n=25 values corresponding to the 5-

652

repeated 5-fold cross-validation performed for each model.

653 654

Figure 3. Scaled partial dependence plots of the cyanobacteria genera; solid lines equal

655

the median partial dependences of the n=25 models per genus, and corresponding shaded

656

areas are bound by the min and max partial dependences. Y-axes correspond to carbon

657

biomass, but the curves have been min-max normalized by genus to enable comparisons

658

among the genera, making the y-axes unitless. Partial dependence plots for each genus

659

(non-scaled) are included in the Supporting Information. The point clouds included at the

660

top of each panel reflect the densities of the explanatory covariates’ observed values.

661 662

Figure 4. Relative sensitivities of the genera to the explanatory variables; y-axes

663

correspond to relative sensitivity values (unitless).


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20

30

(d) Microcystis

Water temp.

0

10

30

0

10

9

3

8

6

6

tp rotifers po4d

copepods tkn

rotifers tp tp

(a) TKN (mg L−1)

4

22 copepods tkn 3 Figure tkn

nh4d Environmental Sciencenh4d & Technology

(b) TP (mg L−1)

Page 34 of 35

n

(c) Dissolved NH4 (mg L−1) (d) Dissolved PO4 (mg L−1)

0. 16

0. 06 6 0 0. 12 0. 09 9 0

nh4d tripton

color

0. 3 03 0 0. 08

80 0. 00 0 0. 04

0. 10 63 0

tp po4d

tripton tripton

40

20 0. 05 2

90

0. 16 0. 00 0 1

nh4d

po4d

0. 12

00. .008 8

tp po4d

60

30

0

00. .004 4

80

3 63 0

40

20

2 2

0.75

0 1 1

90 90

1.00

c

Qavg

0.50

−1 Qavg −1 wtemp 3 −1 ) TP (mg ) (c) (Dissolved (mg(Ld(−1 )CPU Dissolved ) ) PO4 (mg ) (wtemp f)4Color (g)L Ktripton (m−1) (e)LAverage flow m s ) NH

4

0. 3 10

0

30 .0 0 9

0

10 .0 1 0 30 .0 5 2 0 20 .0 0 6

0. 16 0. 0 00 000

color wtemp

0.

50 0

0. 03 20 0 0 0 5 .08 0. 06 30 0 0. 0.1 1 2 40 0 0 .0 0 9

10 0

0.

.0 4

04. 16 00. 0. 00 00 0

312 0.1 0

tripton Qavg

0.

2

08

0. 05

11

color

0.

000. 04

0. 16 0. 00

0. 12 0. 3 0. 09 09

tripton Qavg

0. 0. 03 03 2 0.08 0. 0. 06 06

0.00

0. 0. 00 00 1 0. 04

0.25

(h) Water temperature (oC)

30 50 0

25 40 0

20 30 0

15 20 0

10 10 0

0

0 4

3

30

2

0 20

30

25

20

115 5

110 0

0 30

0 20

0 10

0

0 50

10 1 0

50

wtemp

wtemp

0.50

00

0

0

30

40

0

0 20

0 10

0

0 4

30

3

2 20 0

101 0

50

0.75

00

0

1.00

0.25

) (( ) ) Color((iCPU ) Copepods

( )

o −1 temperature C

0.75

tp

nh4d

po4d po4d

0.50

33

Anabaena Cylindrospermopsis Planktolyngbya Microcystis Oscillatoria 22

1

90

60

30

0

80

60

40

0

20

1.00

Qavg Qavg

00..0 099

00..0 066

0. 0 33

0. 00

30

9205

0. 10

ACS Paragon Plus Environment 6105 20

0. 05

30 10

0. 16

0. 00 color

2 80 3 0 4

0. 08

0. 12

601

tripton

20 00 30 0 420 0 50 400 0

10

0

0.00

0. 04

0.25

30

25

20

15

430

325

0

22

15

1

tkn tkn

−1

10

rotifers

(h) Water ) (m ()j) Rotifers (mgC L )

−1 g Ktripton mgC L

10

10 0.0 0 20 0 0 0. 0 30 3 0 0. 0 40 6 0 0. 0 50 9 0 0

0. 010

copepods

30

2

5 300.0 5 0

0. 0 08 1 0. 0 12 10 015 0. 16 200.020 00

.0

4

0.00

Page 35 of 35



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