Predicting culturable enterococci exceedances at Escambron Beach, San Juan, Puerto Rico using satellite remote sensing and artificial neural networks

Recreational water quality monitoring programs exist worldwide to protect humans from potential exposure to pathogens and are based upon fecal indicator bacteria (FIB; Colford et al. 2007). The FIB monitored varies across latitudes and water types, where Escherichia coli, fecal coliforms, and Enterococcus spp. are most common (Colford et al. 2007; U.S. EPA 2012), and can be correlated with illness in areas with known fecal contamination sources at temperate latitudes (e.g. ∼33.4 °N–37.8 °N; Colford et al. 2012; Boehm & Sassoubre 2014). In the USA, the Environmental Protection Agency (U.S. EPA) monitors Enterococcus spp. in recreational marine waters. Based on the 2012 Recreational Water Quality Criteria (RWQC), enterococci cannot exceed the geometric mean of 35 colony forming units (CFU) per 100 mL, which represents 36 illnesses per 1,000 primary contact recreators (U.S. EPA 2012). This value was then modified to 70 CFU/100 mL based on the Beach Action Value (BAV), recommended by the U.S. EPA National Beach Guidance and Required Performance Criteria for Grants (U.S. EPA 2014). These guidelines were adopted by the Puerto Rico Environmental Quality Board (PREQB), where they monitor recreational water quality around the island of Puerto Rico biweekly in accordance with the 2000 U.S. Beaches Environmental Assessment and Coastal Health Act (U.S. EPA 2000; Cordero et al. 2012) and other water quality standards of Puerto Rico (PREQB 2010).

Escambron Beach is located in San Juan, Puerto Rico and is one of the most visited beaches in the region. Escambron Beach is within the Rio Piedras watershed (Diaz 2007; Lugo et al. 2011) and has a stormwater drainage outfall (18.46 °N, 66.09 °W), which discharges rainwater, agricultural runoff, and other greywaters (Diaz 2007). This FIB point source and the Bayamon Regional and Puerto Nuevo Regional wastewater treatment plant (WWTP; primary wastewater treatment) ocean outfall, located 5 km offshore, are the most prominent point sources of fecal pollution at the beach (Ortiz-Zayas et al. 2006). The nearby Rio Grande de Loiza river mouth also discharges human and non-human fecal pollution to the coastline (Quiñones 2012). In addition to the impact of known fecal pollution sources, culturable enterococci concentrations are influenced by environmental factors (Sanchez-Nazario et al. 2014; Laureano-Rosario et al. 2017). Such factors include: precipitation through increased runoff (Cordero et al. 2012); solar radiance bacterial inactivation (Maraccini et al. 2012, 2016); turbidity being a source of FIB or protecting them from ultraviolet (UV) light (He & He 2008; Shibata et al. 2010); and the resuspension of FIB in sediment reservoirs through increased winds and waves (Byappanahalli et al. 2012; Feng et al. 2013).

Predicting when FIB exceed water quality criteria has been a management goal, and researchers have approached this using a variety of mathematical methods (e.g. linear and nonlinear statistical modeling). Some studies have applied linear models to understand FIB relationships with environmental factors; however, these complex interactions may not be adequately characterized by linear models, which typically describe less than 50% of the variability (Gonzalez & Noble 2014; Laureano-Rosario et al. 2017). Furthermore, previous modeling efforts lacked infrastructure and human activities data (i.e. land use); consequently, they did not accurately predict FIB concentrations (Rochelle-Newall et al. 2015). FIB vary depending on location, sources, and environmental factors; thus, a nonlinear approach is more appropriate due to FIB complexity and their relationship with multiple parameters. Thus, nonlinear modeling is essential to understanding the complex relationships between environmental variations and FIB.

Studies using nonlinear methods, mostly based on machine learning, focused on relationships between FIB and environmental factors to predict recreational water quality (He & He 2008; Thoe et al. 2014; Avila et al. 2018; Zhang et al. 2018). These studies used different methods, such as artificial neural networks (ANNs), Bayesian models, decision trees, and Monte Carlo approaches to predict recreational water quality in both marine and freshwaters (Jiang et al. 2013). These models take into account non-continuous relationships by creating a nonlinear combination of predictors to assess their relationship with FIB. For example, Choi & Bae (2018) applied ANNs and predicted total coliform concentrations in California based on rainfall and streamflow. Similarly, Ostad-Ali-Askari et al. (2017) applied ANNs and modeled nitrate pollution as the main water quality indicator in Iran. Furthermore, the ANNs models used in our study were previously compared to decision trees, where it was found that the ANNs approach allowed the specification of the relative importance of false positives and false negatives, whereas the decision tree methodology only provided a fixed operating point (Duncan et al. 2013a, 2013b). Therefore, our study helps fill research gaps in the Caribbean for recreational water quality predictions using ANNs in the context of environmental variability.

Since ANNs are self-driven data-adaptive methods, they can identify nonlinear, functional relationships between FIB and environmental factors. Forecasting recreational water quality can greatly improve the management of recreational waters as managers can overcome the time-lag associated with routine beach water quality monitoring (Enns et al. 2012; Thoe et al. 2014).

Even though ANNs have been widely applied to predict bathing water quality throughout the world, our study expands on this by using long-term satellite-derived data together with in situ bacterial sampling in Puerto Rico. Satellite-derived data has been used to study both land and the ocean for management purposes (McCarthy et al. 2017). These have provided data since the 1980s, allowing long-term studies regarding environmental variability. When it comes to beach water quality, these datasets have not been fully applied to predict bathing water quality, where satellites can provide long-term environmental data that can be combined with monitoring programs that have been in place for more than 10–15 years. There have been a few studies looking at specific satellite-derived data (e.g. sea surface temperature, turbidity) in temperate and tropical areas (Kim et al. 2014; McCarthy et al. 2017; Zheng & DiGiacomo 2017). These have helped show the applicability of satellites; however, there are still some research gaps regarding the combination of satellite-derived data with predictive models in tropical areas. Therefore, this study implemented an ANNs approach, based upon 10 years of culturable enterococci concentration data together with in situ and satellite-derived environmental data, to predict recreational water quality at Escambron Beach, San Juan, Puerto Rico. More specifically, the model was developed using satellite-derived direct normal irradiance (DNI), turbidity, sea surface temperature (SST), and dew point with local observations of mean sea level (MSL), and cumulative precipitation from 24 h up to 120 h. The objectives of this study were: 1) to identify the most relevant environmental factors to predict culturable enterococci RWQC exceedances at Escambron Beach from 2005–2014; 2) to show the applicability of nonlinear modeling for an early warning system based on ANNs; and 3) show the benefit of incorporating remotely sensed data.

The results of this study can help understand the applicability of satellite-derived data in early warning systems and predictive models and the complex relationship between environmental factors and FIB in the Caribbean, with the aim of predicting exceedances and helping with management and mitigation of recreational water quality standards.

This study took place at Escambron Beach (Figure 1), one of the most popular beaches of San Juan, Puerto Rico (18.47°N, 66.08°W). This beach has a year-long swimming season. The municipality of San Juan (17.92°N–18.52°N, 65.62°W–67.28°W) has a tropical climate. Escambron Beach is classified as a low wave action beach, with mixed semidiurnal tides. Currents around the study area are generally westward; however, the Caribbean Coastal Observing System (CariCOOS; www.caricoos.org) buoy's current data shows very weak south-southeast semi-diurnal tidal currents on Puerto Rico's northern coast between 2 and 30 m depth. In San Juan, the annual average precipitation is ∼1,800 mm, and average air surface temperatures range between 24 and 29 °C. The study area is potentially influenced by the following sources of fecal pollution: stormwater outfall (Diaz 2007), the Rio Grande de Loiza river (Ortiz-Zayas et al. 2006; PREQB 2007), San Juan Bay Estuary (Perez-Villalona et al. 2015), and the Bayamon and Puerto Nuevo Regional WWTP ocean outfall (Ortiz-Zayas et al. 2006; PREQB 2007, 2011).

Culturable enterococci data for Escambron Beach were downloaded from the U.S. National Water Quality Monitoring Council from 2005 to 2012 (NWQC 2017). Data were for two sites separated by a distance of ∼100 m; these were pooled due to their proximity and satellite data resolution. This dataset was extended from 2012 to 2014 with data provided by PREQB; thus, a total of 10 years of data were used (n= 273 observations for both sites combined). The culturable enterococci data were generated by the PREQB using U.S. EPA method 1,600 and had a detection limit of 4 CFU/100 mL. All enterococci concentrations described as below the limit of detection were substituted by the next highest concentration (e.g. 3 CFU/100 mL; Laureano-Rosario et al. 2017). Bacterial sampling was biweekly (i.e. every other week) and the combined geometric means from both sampling sites, commonly used due to bacterial variability, were then calculated. These geometric means were used in all further analyses.

Daily precipitation data (in situ) were obtained from the U.S. National Oceanic and Atmospheric Administration (NOAA) National Center for Environmental Information from 2005 to 2014. DNI and dew point were obtained from the satellite-derived U.S. National Solar Radiation Database (2005–2014; 30-min temporal resolution and 4 km spatial resolution). Daily MSL was obtained from the University of Hawaii Sea Level Center from 2005 to 2014. These datasets are obtained from a tide gauge located ∼2 km from our study site. Day- and night-time SST were obtained from the U.S. NOAA Advanced Very High Resolution Radiometer (1 km spatial resolution) from 2005 to 2014. Data were extracted using the average of three 3 × 3-pixel boxes, for the north coast of San Juan, Puerto Rico. Interactive Data Language (IDL; v. 7.2) was used to extract data. Remote sensing reflectance at 645 nm (R_rs 645; Chen et al. 2007) was used as a proxy for turbidity from the NASA Moderate Resolution Imaging Spectroradiometer (MODIS-Terra; 250 m spatial resolution). Data were extracted using MATLAB (v. 2014b; The MathWorks Inc., Natick, MA, 2000); the average of two 3 × 3-pixel boxes was used for turbidity for this coastal region. The environmental variables included in the model to predict culturable enterococci exceedances were: MSL, cumulative precipitation for 24, 48, 72, 96, and 120 h, SST, DNI, dew point, and turbidity. All satellite-derived data images corresponded to 1-day point samples. These images were compared with in situ collected data, where they followed similar patterns. All input variables were log-transformed for predictive purposes.

ANNs calculate weights and biases to understand strengths and relationships between inputs and outputs (Basheer & Hajmeer 2000; Duncan et al. 2013a, 2013b). ANN weights were calculated for the hidden layers (W₁) and the output layer (W₂; Figure 2). The final weights (W₀) were calculated through matrix math of the ANNs hidden layer weights matrix and ANNs output layer weights vector (i.e. W₁ · W₂ = W₀; Duncan et al. 2013a, 2013b; Duncan 2014). These final weights values were used to identify the most relevant parameters through NPSFS to predict culturable enterococci concentration exceedances. Members of the ensemble were trained on a similar but different subset of the full training dataset. Therefore, weights obtained in each ANN had different values. For a single output ANN, the result was a vector that specified the combined pathway strength of each input on the output. Combined Neural Pathway Strength Analysis (CNPSA) was used to identify if the relationships were excitatory or inhibitory (Basheer & Hajmeer 2000). In that case, the input is considered relevant to predict enterococci exceedances. The model was run as categorical, where it identified either a pass or fail. The model used binary coding to classify passes (1) and fails (0). Therefore, when classified as excitatory it meant bacteria would pass (i.e. below threshold) and when classified as inhibitory it meant that bacteria would fail (i.e. above threshold).

Crossover and mutation rates, incorporated by NSGA-II during the training period, were used to optimize weights. These crossover and mutation rate factors differentiated new weights generations from the parent generation (Duncan 2014). Different crossover and mutation rate input values were tested; however, the crossover rate used was 0.2, and the mutation rate was 0.1. These input rates were used as they provided the best optimization results during the predictions of exceedances. Model's cost function used false positive rates and false negative rates. We used the minimum Euclidean distance to an ideal true positive ratio equal to one; these distances were derived from the ROC and used for optimization by NSGA-II to assess the quality of solutions (Duncan et al. 2013a, 2013b; Duncan 2014). Data were divided into ten epochs to ensure that the data used for training and validation were different than the data used for testing predictions as follows: epochs 1–3, 5, and 7 for training (n = 152); epochs 4, 6 and 8 for validation (n = 66); and epochs 9 and 10 for testing (n = 55).

To predict when enterococci exceeded the PREQB RWQC for safe recreation, the threshold selected for this study was the geometric mean concentration of 70 CFU/100 mL (PREQB 2016). This concentration is the BAV recommended by the U.S. EPA to ensure no more than 36 illnesses per 1,000 recreators and was adopted by the PREQB in 2015 (U.S. EPA 2014; PREQB 2016). The model compared the observed and predicted enterococci concentrations to this BAV threshold and identified them as ‘safe for swimming’ (i.e. below threshold) and ‘potentially unsafe for swimming’ (i.e. above BAV threshold). Results showed the influence, and magnitude, of inputs to predict enterococci exceedances based on the specific thresholds mentioned above. These are shown as inputs having an inhibitory or excitatory influence on outputs crossing the set thresholds. Based on the 70 CFU/100 mL, we had a total of 238 passes, and 35 fails in the original data.

The model predicted culturable enterococci exceedances with an accuracy band of 76% for Escambron Beach during 2005–2014 based on all ensemble models. This accuracy represented how many correct versus incorrect predictions were obtained compared to observed values. Overall, the model accurately predicted culturable enterococci exceedances based on the PREQB RWQC for safe recreation, with a power greater than 60%, where the FM was 0.61, and the AuC was 0.74 (Figure 3). Both FM and AuC provided the specificity and sensitivity of the model as these were based on the a-factor discussed above and the optimum Euclidean distance from the ideal point (i.e. False Positive Rate = 0 and True Positive Rate = 1; Duncan 2014).

The most relevant parameters to predict culturable enterococci concentrations at Escambron Beach from 2005 to 2014 were DNI, turbidity, 48 h cumulative precipitation, MSL, and SST (Figure 4). Only MSL and DNI showed an excitatory relationship; whereas turbidity, 48 h cumulative precipitation, and SST showed an inhibitory relationship. The most relevant variables were DNI and turbidity, where DNI showed a smaller spread of weights compared to turbidity. These environmental factors were identified as showing either an excitatory (positive weights) or inhibitory (negative weights) influence based on the binary coding. For example, DNI had an excitatory influence on predicting enterococci exceedances (Figure 4), which represented an overall stimulus of DNI on culturable enterococci concentrations not to cross the BAV threshold, meaning the results would be a pass (or binary code 1). This represents a negative correlation between DNI and culturable enterococci, where it inhibits the bacterial cell to cross the BAV value. On the other hand, turbidity showed an inhibitory influence, meaning that it influences bacterial concentration to cross the BAV threshold, representing a fail (or binary code 0). This represents a positive correlation between turbidity and culturable enterococci, where it promoted higher concentrations that crossed the set threshold. Weight distributions were used as indicators of relevancy (Duncan 2014), where it was found that six variables (i.e. cumulative 24 h precipitation, cumulative 96 h precipitation, date, cumulative 120 h precipitation, and dew point), which crossed the zero line of the box and whisker plots, were not considered relevant to predict culturable enterococci exceedances at Escambron Beach surface waters for this time period.

This study investigated the use of satellite-derived data and a nonlinear model to predict exceedance of the PREQB RWQC for safe recreation at Escambron Beach, San Juan, Puerto Rico. The most relevant variables in this model were DNI, turbidity, cumulative 48 h precipitation, MSL, and SST. These results showed that accurately predicting culturable enterococci exceedances, based on the 2014 BAV value, at Escambron Beach can be achieved using the aforementioned environmental variables. Notwithstanding, this model could make improved predictions by including a larger dataset and geo-referenced sanitation infrastructure data.

The ANN modeling described in this study showed the importance of identifying how environmental conditions can influence culturable enterococci concentration, as well as the complexity of these relationships between FIB and environmental factors. The use of ANNs to model culturable enterococci concentrations at Escambron Beach provided an accuracy band of 76% for exceedances, with greater than 60% model power, which is higher than previous models using linear approaches (e.g. Laureano-Rosario et al. 2017), and similar to those using ANNs for FIB predictions (e.g. He & He 2008; Chebud et al. 2012). Modeling enterococci exceedance at Escambron Beach was achieved by using the U.S. EPA and PREQB BAV (70 CFU/100 mL) as the model threshold concentration. By using this threshold, the model identified 35 occasions in which enterococci concentrations exceeded the BAV (i.e. model fails) in the original data and these events were then used for predictive purposes. AuC and FM provided the model's power and accounted for the ratios of true positives and true negatives. The accuracy band accounted for predicted values individually compared to the original values. These percentages may be affected by the number of passes (n = 238) and fails (n = 35) in the original observations.

These results also showed the applicability of combining satellite-derived data with nonlinear modeling. Sampling of monitoring programs usually is biweekly, which can greatly affect predictive power due to lower data resolution. Satellite remote sensing data can provide data once or twice a day depending on the sensor. For example, AVHRR provides SST data in the morning and afternoon. MODIS sensors also provide data in the morning (∼10:30 AM; Terra satellite) and the afternoon (∼1:30 PM; Aqua satellite). These datasets are freely available and are an important addition to management strategies if combined with monitoring programs that have been in place (McCarthy et al. 2017). These monitoring programs also help validate satellite-derived data.

Parameterization of the model was achieved with satellite-derived data as these provided larger datasets to be used during training, testing, and validation on the ANNs. Data were divided into a series of ANNs ensembles, and sensitivity and specificity were achieved by using FM and AuC. These were also possible by the inclusion of satellite-derived data, especially for products such as DNI and turbidity as they are not collected during every sampling effort. Therefore, by including satellite-derived data, it shows how models can be improved with better data resolution and potentially reducing sampling efforts (McCarthy et al. 2017).

Despite the high model power observed, future studies could improve upon the model created in this study by considering FIB watershed sources and longshore currents sources. For example, it is likely that failing sanitation infrastructure (e.g. leaky sewer pipes and septic systems) influenced FIB at Escambron Beach (Naidoo & Olaniran 2014). Additionally, WWTP, as well as stormwater discharges, could be a potential source of FIB throughout the year at various levels, and future studies should take them into account. Lastly, climatic conditions vary annually, and this natural variability can affect enterococci predictions over time.

The presence of enterococci in beach sands and vegetation (e.g. seagrass, green alga; Whitman et al. 2003; Sanchez-Nazario et al. 2014; Halliday et al. 2015) should also be considered to understand how these non-fecal sources influence enterococci concentrations (Feng et al. 2012, 2013). Thus, predictive models can likely be improved by the inclusion of these data. Furthermore, there is also the need to identify other factors that might be of importance (e.g. through microbial source tracking, different fecal indicators, infrastructure data), to better predict these exceedances, identify when those are related to human fecal contamination versus non-human fecal contamination, and protect public health. Results of this model can potentially be implemented in an early warning system, using those variables identified here as predictors of bathing water quality. These, in turn, can be combined with ANNs, satellite-derived data, and on-going monitoring programs to build now-casting models. Since satellite-derived data has been available for the past 20–30 years, it can help identify specific indicators correlated with FIB and reduced sampling efforts. Nevertheless, these relationships shown here are specific for Escambron Beach and culturable enterococci, and future work should modify and assess other environmental indicators that are correlated with fecal contamination.

Culturable enterococci concentration variability in coastal areas is influenced by fecal pollution sources, secondary, extraintestinal reservoirs, as well as by environmental factors (Viau et al. 2011). The current study accounted for specific environmental factors, such as DNI, turbidity, precipitation, MSL, SST, and dew point. These environmental factors have been shown to influence culturable enterococci concentrations, and other FIB, in temperate and tropical environments as well as marine and freshwaters (Enns et al. 2012; Lamparelli et al. 2015; Aranda et al. 2016).

As regards to environmental variables, precipitation most often explains the majority of FIB variability observed (He & He 2008; Feng et al. 2013; Laureano-Rosario et al. 2017); however, this study identified DNI as the most relevant environmental variable (Maraccini et al. 2012, 2016). The three most influential variables predicting PREQB RWQC exceedance were DNI, turbidity, and 48 h cumulative precipitation. DNI was the most important environmental variable to consider for PREQB RWQC exceedance predictions, likely due to bacterial inactivation (Maraccini et al. 2012, 2016). Since Escambron Beach is located in a tropical setting, it is no surprise that sunlight is one of the most influential environmental factors (Rochelle-Newall et al. 2015). Exposure to UV light results in bacterial inactivation, and consequently a decrease in bacterial concentrations (Byappanahalli et al. 2012; Walters et al. 2014). The next most influential predictive environmental variable was turbidity, which has been documented to protect bacteria from UV light exposure. Turbidity is also associated with increased FIB when precipitation facilitates runoff into coastal waters (Halliday et al. 2015; Aragones et al. 2016). Thus, the combined turbidity and DNI effects on enterococci concentrations could be the reason why these were identified as the most relevant parameters to predict culturable enterococci concentration exceedances.

The third most relevant parameter that predicted culturable enterococci exceedance at Escambron Beach was 48 h cumulative precipitation. He & He (2008) also identified 24–48 h of cumulative precipitation as significantly correlated with FIB at Torrey Pines State Beach and San Elijo State Beach, San Diego County, California, USA. Rainfall is known to increase FIB concentrations due to runoff (Colford et al. 2012), inadequately treated wastewater effluents (e.g. septic seepage; Naidoo & Olaniran 2014), and combined sewer-stormwater systems (He & He 2008). Since a nonlinear modeling approach was used in this study, the previously identified holistic influence of the aforementioned environmental conditions was able to be incorporated into the model, and improved predictions were generated (Noble et al. 2004).

The least two relevant environmental variables associated with PREQB RWQC exceedance predictions at Escambron Beach were MSL and SST. Previously at other beaches in Florida and California, USA, increased MSL was associated with lower culturable enterococci concentrations due to dilution and decreased MSL was associated with higher concentrations due to backwashing of waves and increased discharge into the coastal areas (Maraccini et al. 2012; Feng et al. 2016). However, Escambron Beach is a low-wave action beach, with a minimal tidal range; thus, MSL is not expected to strongly influence enterococci concentrations. Regarding SST anomalies, warmer waters have been documented to increase bacterial replication (Byappanahalli et al. 2012), and consequently, SST warm-anomalies have been shown to be related to increased culturable enterococci concentrations in tropical settings (Pachepsky et al. 2014; Laureano-Rosario et al. 2017). Even though SST was not the most influential environmental variable identified by the model, it still provided information to predict PREQB RWQC exceedances.

This work shows that nonlinear models help to predict water quality with relatively good accuracy (76%). Data availability is an important aspect, especially the information regarding coastal water quality and both anthropogenic and environmental factors, due to their influence on FIB variability and phenology. Thus, a collection of data and water quality monitoring programs are important to better understand FIB variability. Through modeling culturable enterococci concentration exceedances, this study found the following:

• The most relevant parameters to predict culturable enterococci surface water concentrations at Escambron Beach from 2005 to 2014 were DNI, turbidity, cumulative 48 h precipitation, MSL, and SST.

• ANNs were able to predict enterococci concentration exceedances at Escambron Beach with an accuracy of 76% and a power greater than 60%, which is higher than most statistical linear models.

• Among the environmental variables evaluated, DNI, turbidity, and 48 h cumulative precipitation showed the highest influence on predicting culturable enterococci concentrations at Escambron Beach, which represent their holistic influence on enterococci concentrations.

• Only DNI and MSL showed a positive influence, whereas turbidity, 48 h cumulative precipitation, and SST showed an inhibitory (negative) influence on predicting culturable enterococci concentrations at Escambron Beach.

• Model predictive power may be improved by including sanitary survey data (e.g. septic system density), as well as other data describing enterococci sources, such as algal and seagrass coverage, and stormwater and river discharges.

A.E.L.R. was supported by the U.S. National Science Foundation (NSF) Partnerships for International Research (PIRE) under Grant No. 1243510 and by the U.S. National Aeronautics and Space Administration (NASA) Headquarters under the NASA Earth and Science Fellowship Program Grant No. NNX15AN60H. A.E.L.R. was also funded by the USF College of Marine Science Linton Tibbetts Endowed Fellowship. F.M.K. was supported by the U.S. EPA Science to Achieve Results (STAR) grant No. 83519301. E.M.S. was supported by U.S. NSF grant OCE-1566562. We would like to thank the teams from the Universidad Autonoma of Yucatan, Puerto Rico Environmental Quality Board, and Centre for Water Systems for their help and input for this work. We would also like to thank the IMaRS team for their input and help in manuscript revisions.