Temporal variability of enterococci and associated sources at three subtropical recreational beaches

Recreation is an ecosystem service that best represents beaches. It supports a growing tourism activity that generates jobs and revenue, thus fostering economic development. However, evidence from epidemiological studies and quantitative assessments of the microbial infection risk by recreational exposure to beach water shows an overall high risk of gastrointestinal diseases (Fewtrell & Kay 2015). Tourist exposure to unhealthy beaches has been estimated to cause ~120 million cases of gastrointestinal disorders and ~50 million cases of respiratory diseases per year (Shuval 2003). Thus, the concept of the beach as a microbial habitat and a reservoir of fecal bacteria and pathogens has begun to influence our thinking about the exposure to and recreational use of beach water and sand and their effects on human health (Whitman et al. 2014).

The main sources of fecal contamination on beaches are wastewater discharges, river discharges, and bathers (defecation and/or shedding). Other sources include septic tanks in the vicinity of beaches, animal stools, deposition of airborne pathogens, maritime traffic, as well as transport of fecal bacteria by rain, wind, tides and currents (Praveena et al. 2013; Tilburg et al. 2015). It is usually difficult to relate particular sources to health risks due to the diverse nature of the sources of fecal indicator bacteria, the discharge processes and their destination, as well as the scarce estimates in many watersheds (Huang et al. 2017). Therefore, for a given beach, all potential sources should be examined and more research efforts should be devoted to better understand the variability of fecal indicator bacteria.

The microbiological quality of beach water is commonly assessed using fecal indicator bacteria, including total coliforms, fecal coliforms, E. coli, and enterococci (Oliveira et al. 2016). The World Health Organization has established public health risk criteria based on the concentration of enterococci in seawater on beaches (WHO 2003). This is based on the tolerance of enterococcus bacteria to saline environments and the fact that their concentration in water is positively correlated with the incidence of respiratory or gastrointestinal diseases as well as eye and ear infections in bathers (Cabelli et al. 1982; Pruss 1998; Haile et al. 1999). Sand, the other major component of beach recreation, has not been included in the current monitoring and regulation schemes. Both the surface and porous spaces between sand grains provide suitable conditions for the survival, reproduction and viability of microbial populations, and the importance of beach sand for public health has been extensively documented (Heaney et al. 2014; Whitman et al. 2014; Zhang et al. 2015). Despite the lack of quantitative criteria, it is recommended to monitor the quality of beach sand in order to gather information for standard protocols and to define assessment criteria (Sabino et al. 2014).

It has been observed that an increase in the influx of beach users leads to an increase in enterococci density, indicating fecal contamination, which may be favored by inadequate, insufficient or inefficient sanitation infrastructure (WHO 2003). A better understanding of microbiological quality and the beach surroundings is essential for assessing the implications for human health (Quilliam et al. 2015).

This study aimed at examining the variability of enterococci concentrations in water and sand at three subtropical recreational beaches. Based on this, we have assessed the public health risks during the seasons with a contrasting influx of beach users, taking into account the prevailing wind, rain and water conditions.

The three studied beaches, Los Algodones, San Francisco and Miramar, showed a similar variability pattern in the concentration of enterococci in water: low concentrations (< 100 MPN 100 ml⁻¹) before the Easter Week, high concentrations (> 1500 MPN 100 ml⁻¹) during and immediately after the Easter Week and decreasing, although always > 200 MPN 100 ml⁻¹, concentrations during the wintertime. Thus, health risks for users of these beaches are higher during and after the Easter Week.

Before the Easter Week, the sanitary quality of water at the three beaches was suitable for primary contact recreational use, the number of users was low < 40, and there was no rainfall. The highest influx of users at the three beaches (~96% of the total number of visitors throughout the study period) was observed for a period of approximately 10 days during the Easter Week. This coincided with the time when the highest enterococci concentrations (> 1500 MPN 100 ml⁻¹) were recorded. The lack or insufficiency of sanitary services (García-Morales et al. 2018) on these beaches, combined with the fact that most visitors camp out on the beach during the Easter Week, suggest that the high influx of users is the main source of fecal contamination, reaching levels that pose a threat to public health. This matches with other studies that have shown that the influx of users can be identified as the root cause of fecal contamination in beach water (Fattal et al. 1991; Fleisher et al. 2010). It is therefore important to assess the number and distribution of visitors on the beaches. The analysis of such data provides information useful for environmental and public health management (Dwigth et al. 2007), including investment in the construction of sufficient sanitation infrastructure.

The influx of users decreases significantly after the Easter Week, but the level of enterococci in the water remains high. This may be explained as follows: (1) enterococci populations established during the Easter Week still remain in the medium, (2) the effect of runoff from rain that fell prior to sampling at this time, and (3) the observed increase in water temperature (26–29°C). The populations of enterococci established during the Easter Week may persist as they are able to attach to zooplankton in seawater (Signoretto et al. 2004). The rainfall runoff is an important source of enterococci as it carries materials from land to the sea (Tilburg et al. 2015; Huang et al. 2017). This effect is more pronounced in the case of urban beaches, as observed at our urban beach (Miramar), where higher concentrations of enterococci were recorded compared to the other two less urbanized beaches. In addition, untreated municipal wastewater is discharged in the Miramar surroundings, which increases the fecal contamination. Furthermore, fecal contamination of beach water at this time of the year is facilitated by the fact that enterococci thrive at temperatures ranging from 10°C and 45°C and their development and persistence on these beaches is thus favored by the water temperature rise (Byappanahalli et al. 2012) that takes place after the Easter Week, reaching 25–30°C. The conditions prevailing on these beaches during the summer, namely the peak of the rainy season (Fig. 2), water temperature ~29°C (Mitchell et al. 2002), and the high influx of users (Garcia-Morales et al. 2018) suggest that the public health risk persists throughout the summer.

The concentrations of enterococci in water during the wintertime were > 200 MPN 100 ml⁻¹, which is indicative of a human health risk. Although enterococcus bacteria grow better at high temperatures, they can withstand adverse conditions in the marine environment, which makes them excellent indicators of fecal contamination on beaches (Hanes & Fragala 1967; Noble et al. 2003). This accounts for their presence in the wintertime when water temperature was ~18°C. At this time of the year, when there is a low influx of visitors, the likely sources of fecal contamination are winds, migratory seabirds and domestic animals. The results of the wind analysis showed that the prevailing winds in the area are W–NW with a speed of 18–22 km h⁻¹, which carry dust from land to the sea. It should be noted that in this semi-arid subtropical coastal zone, the surrounding vegetation of shrublands and shrubs favors an effective transport of dust from land. In winter, the presence of migratory birds and pets on these beaches or in their vicinity gives rise to the hypothesis that they represent additional potential sources of fecal contamination. Enterococci brought in by seabirds may play a major role on Miramar and San Francisco beaches due to their location near the estuaries and mangrove forests that provide habitats for thousands of migratory birds in this region of the Gulf of California (Anderson et al. 1976), thus increasing the contribution of excreta. In this regard, Byappanahalli et al. (2015) used molecular markers to show that most fecal contamination on a Chicago beach came from shorebirds (geese and seagulls). In particular, San Francisco Beach is extensively used by visitors to walk dogs (Garcia-Morales et al. 2018), and there is evidence suggesting that dogs are the major source of enterococci on the beach. A comparison of enterococci sources showed that a single dog fecal event is equivalent to 6940 bird fecal events, while a single human adult contributes approximately the same as a bird fecal event (Wright et al. 2009). The limitation of this study is that the number of dogs and birds on the beaches was not counted and this should be considered in future studies.

On the other hand, the concentration of enterococci in sand was lower compared to beach water. This can be attributed to their transport on bather bodies after contact with water. This is the basis of hygiene rules when using swimming pools, as it is believed that showering before entering the pool removes germs and substances that can be transported on the body. This is not practiced by users of the surveyed beaches, as there is no shower on any of the beaches.

The concentration of enterococci on the three studied beaches was higher in dry compared to wet sand, which coincides with observations for other beaches: Lauderdale Beach, Hollywood Beach, and Hobie Beach, South Florida (Bonilla et al. 2007), and three beaches located in the South Coast region of São Paulo State, Brazil (Pinto et al. 2012). Also Mudryk et al. (2014) observed that dry sand on a recreational beach in the southern Baltic Sea was inhabited by the largest number of potentially human pathogenic bacteria.

The highest concentrations of enterococci were recorded during and after the Easter Week, which was clearly associated with the same sources of enterococci in water for this time of the year (influx of visitors, rainfall and water temperature). In general, enterococci concentrations in sand were < 200 MPN 100 ml⁻¹, except for one sampling at San Francisco Beach where the concentration exceeded 500 MPN 100 ml⁻¹. This finding can be accounted for by runoff. In the wintertime, enterococci concentrations in sand were < 25 MPN 100 ml⁻¹, with the highest concentration recorded at Miramar Beach – the urban beach affected by untreated wastewater. Given the prevailing wind direction and speed, the low enterococci concentrations in dry sand during the winter can be attributed to wind action that transports surface sand toward the sea.

Mexican regulations for the sanitary assessment of beaches only requires the determination of enterococci concentration in water. However, the presence of enterococci in sand may also pose a public health hazard, as this is the part of the beach where users spend most of their time. According to Heaney et al. (2014), it is also important to better understand to what extent people are exposed to fecal bacteria in sand, the environmental factors that control their occurrence and distribution in sand, and their connection with the concentration of fecal bacteria in water.

Although the three beaches showed a similar variability pattern in enterococci concentrations, Miramar poses higher public health risks as, in addition to the direct impact of users, it is affected by untreated wastewater discharges and urban surroundings. San Francisco Beach lacks sanitation infrastructure, which increases the risk of fecal contamination by users. Although there are some hotels and restaurants in the vicinity of Algodones Beach, the beach itself does not have any public sanitation facilities. The Mexican government has been implementing the National Clean Beaches Program since 2003, which includes 268 beaches, 38 of which are certified according to relevant Mexican regulations and 33 hold the Blue Flag certification. The three surveyed beaches, Algodones, San Francisco and Miramar, are included in the Clean Beaches Program but they lack any certification (CONAGUA 2017).

The results of our study on the seasonality, concentration and variability of enterococci on recreational beaches in the subtropical semi-arid region are useful to raise public awareness about certain periods of the year when greater risks of disease occur. However, according to Byappanahalli et al. (2012), epidemiological studies including the identification of enterococcus bacteria at the species level and the quantification of pathogens are necessary to better understand the public health risks associated with high enterococci concentrations.

The results of this study showed that users of the beaches (Algodones, San Francisco and Miramar) are exposed to different levels of health risk depending on the season of the year. The highest risk occurs during and after the Easter Week when the concentrations of enterococci in water show values > 1500 MPN 100 ml⁻¹. An intermediate health risk is associated with the winter period when concentrations ranged from 200 to 500 MPN 100 ml⁻¹, while the lowest risk is before the Easter Week (< 100 MPN 100 ml⁻¹). As evidenced by our study, the main enterococci sources come from the high influx of users during the Easter Week, the rainfall runoff, and the rise in water temperature particularly after the Easter Week. Other important sources seem associated with the prevailing winds and the presence of dogs and birds in winter. The concentrations of enterococci in sand (both dry and wet) showed similar patterns to those in water, however, the values were generally < 200 MPN 100 ml⁻¹ and they were higher in dry compared to wet sand. This represents an intermediate health risk to users, even those that do not go to the sea for swimming.

The three subtropical beaches studied, Algodones, San Francisco and Miramar, showed a similar variability pattern in the concentration of enterococci in water, with the lowest concentrations (< 100 MPN 100 ml⁻¹) and therefore a low health risk being recorded before the Easter Week. In winter, the concentrations ranged from 200 to 500 MPN 100 ml⁻¹, representing an intermediate health risk level during this period of the year. However, the highest concentrations (> 1500 MPN 100 ml⁻¹) and consequently the high health risk occurred during and after the Easter Week. This study provides evidence that sources of enterococci accounting for this variability pattern are the high influx of users during the Easter Week, rainfall runoff, the rise in water temperature after the Easter Week and, according to our hypothesis, prevailing winds and the presence of dogs and birds in winter. The concentrations of enterococci in sand were generally < 200 MPN 100 ml⁻¹ and they were higher in dry sand compared to wet sand. The concentrations were higher during and after the Easter Week; the same pattern was determined for water.

This information on semi-arid subtropical beaches may be a useful reference when comparing the factors that control the abundance of enterococci and its variability on temperate and tropical beaches. It may also support decisions and efforts to prevent public health risks and maintain the recreational and tourism ecosystem services provided by the beaches. The suggested actions to prevent fecal contamination include increasing the number of restrooms, eliminating sewage discharges, controlling access of pets, monitoring sanitary quality of sand and water throughout the year, and informing beachgoers about the sanitary condition of the beaches.