SciELO - Scientific Electronic Library Online

 
vol.47 número3Variabilidad espacial y estacional de temperatura, salinidad y densidad en Bahía Concepción, Golfo de California, MéxicoInfluencia de la península de Mejillones en la variabilidad oceanográfica anual e interanual frente al norte de Chile índice de autoresíndice de materiabúsqueda de artículos
Home Pagelista alfabética de revistas  

Revista de biología marina y oceanografía

versión On-line ISSN 0718-1957

Rev. biol. mar. oceanogr. vol.47 no.3 Valparaíso dic. 2012

http://dx.doi.org/10.4067/S0718-19572012000300012 

Revista de Biología Marina y Oceanografía
Vol. 47, Nº3: 503-512, diciembre de 2012
Article

ARTÍCULOS

Abundance and distribution of fecal indicator bacteria in recreational beach sand in the southern Baltic Sea

Abundancia y distribución de indicadores bacterianos fecales en playas arenosas recreacionales en el sur del Mar Báltico

 

Piotr Skórczewski1, Zbigniew Mudryk1, Joanna Gackowska1 and Piotr Perlinski1

1Department of Experimental Biology, Pomeranian Academy in Slupsk, Arciszewskiego 22 B, 76-200 Poland
pperlinski@apsl.edu.pl


RESUMEN

Se estimó la densidad y la distribución de indicadores bacterianos fecales en arena seca y húmeda y en el agua de mar adyacente de una playa marina recreacional de Polonia en el Mar Báltico. El número de coliformes totales, coliformes fecales y estreptococos fecales fueron entre 3 y 9 veces mayores en la arena seca que en el agua de mar y entre 2 y 6 veces mayores en arena seca que en arena húmeda. Dentro de un año, el número de bacterias fecales que habitaron la arena y el agua de mar mostraron considerables cambios mensuales. El mayor número de indicadores de bacterias fecales en el agua de mar y en la arena aparecieron en la estación de primavera-verano y el mejor estado sanitario se detectó en los meses de invierno. Hubo diferencias en el número de indicadores de bacterias fecales entre la capa de arena superficial y subsuperficial, con una clara tendencia decreciente en el número de las bacterias estudiadas al aumentar la profundidad.

Palabras clave: Mar Báltico, playa, bacterias fecales


ABSTRACT

Density and distribution of fecal indicator bacteria in dry and wet sand and the adjacent seawater of recreational marine beach in Poland, Baltic Sea, were estimated. Numbers of total coliforms, fecal coliforms and fecal streptococci were 3-9 times higher in dry sand than in the seawater and 2-6 times higher in dry sand than in wet sand. Within a year, number of fecal bacteria inhabiting the sand and seawater showed considerable monthly changes. The highest number of the studied fecal indicator bacteria in the seawater and sand occurred in spring-summer season and the best sanitary state was noted in the winter months. There were differences in the numbers of fecal indicator bacteria between the surface and subsurface sand layer with a clear decreasing trend in the number of the studied bacteria with increasing depth.

Key words: Baltic Sea, beach, fecal bacteria


INTRODUCTION

In recent years increased fecal contamination of the sand of many recreational marine beaches was observed, which consequently results in an increased risk of illness among beach users (Elmir et al. 2007, Stewart et al. 2008, Heaney et al. 2009). The sand of beaches acts as a passive element of cumulative pollution accumulating fecal bacteria from point sources such as municipal wastewater effluents, and non-point sources such as recreational users, fecal droppings from wild animals (mainly birds), agricultural run-off, storm drain and mats of green algae (Craig et al. 2002, Sato et al. 2005, Edge & Hill 2007). According to Shibata et al. (2004) and Bonilla et al. (2007) the accumulation of fecal bacteria in sand has two potential consequences for beach users. The washout of bacteria from the sand into nearshore waters might complicate the task of water quality managers' intent on monitoring the quality of bathing water. Moreover, if fecal indicators are being concentrated in beach sand, fecal-borne pathogens may also be accumulating raising the question of whether contact with sand poses additional health risks related to beach use. Numerous studies (Hartz et al. 2007, Heaney et al. 2009, Yamahara et al. 2009, Griffith et al. 2010) found that the conditions in foreshore, nearshore and backshore sand of marine beaches can favour the persistence, survival and regrowth of fecal indicator bacteria. The large surface area of sand grains and the unique microhabitats within the cracks and crevices provide microbes with variety of potentially suitable environments for enhanced survival and growth (Craig et al. 2004, Bonilla et al. 2007). Whitman & Nevers (2003), Byappanahalli et al. (2006) and Brownell et al. (2007) showed that bacterial fecal indicators can persist in sand throughout the year with little variation in counts. Therefore, sand of marine beaches may be an important reservoir of metabolically active fecal bacteria (Hartz et al. 2007).

Total coliforms, fecal coliforms and fecal streptococci are the main organisms indicating the possibility of fecal contamination of recreational water and sand of marine beaches (Shibata et al. 2004). Their presence indicates the potential presence of pathogenic bacteria and is a good predictor of health risks related to marine beach use (Colford et al. 2007, Griffith et al. 2010). Studies on abundance and distribution of fecal bacteria in marine beaches are necessary to understand their potential threat to human health and correctly target fecal pollution prevention actions (Edge & Hill 2007, Stewart et al. 2008). For that reason the aim of the present study was to determine number and distribution of total coliforms, fecal coliforms and fecal streptococci in sand and the adjacent seawater in recreational marine beach in Ustka located at the southern Baltic Sea.

 

MATERIALS AND METHODS

Study area and sampling

The study was carried out on non-tidal sandy beach (54° 35`N and 16° 51`E) localized in Ustka town, Poland (southern Baltic Sea) (Fig. 1). It is located at the mouth of the River Slupia, which divides the studied beach into two parts: Eastern Beach and Western Beach. It represents a dissipative beach type with longshore bars and troughs and its width is about 75 m. In general, the beach is fine and medium-grained, and the sand grain-size is between 0.125 and 0.250 mm (Kramarska et al. 2003). The studied beach, particularly in autumn and winter, is exposed to strong winds that generate high waves, which cause strong erosion onshore. As a result the seashore along the Ustka beach is heavily destroyed and the coastline retreats on average 0.08 m every year (Zawadzka-Kahlau 1999). There are two main sources of contamination of this beach: the River Slupia and seabird/shorebird populations.

Dry and wet sand and seawater samples were collected bimonthly between November 2007 and October 2008 at Eastern Beach. Samples of sand were obtained from two sites along a profile perpendicular to the shoreline (Fig. 1). Wet sand was collected from a site situated at the waterline and dry sand was collected from a site located a halfway up the beach at a 30 m distance from the shore. Sand core samples were taken with a hand operated sampler (length 30 cm, inner diameter 15 cm). In the field, sand samples were divided into two sections: 0-5 cm and 10-15 cm and placed in sterile plastic jars. Seawater samples were collected in sterile bottles within a 1.5 m from the waterline at a depth of about 15 cm. Jars and bottles were put into containers with ice and transported to the laboratory. The time between sample collection and bacteriological analyses did not usually exceed 2-3 h.

 

Figure 1. Location of sampling sites on the sandy beach in Ustka, Poland
Figura 1. Ubicación de los sitios de muestreo sobre la playa de arena en Ustka, Polonia

 

Bacteriological analyses

All collected sand and seawater samples were tested for the number of total coliforms (TC), fecal coliforms (FC) and fecal streptococci (FS). In order to determine the number of fecal indicator bacteria, 5.0 g of sand samples were weighed aseptically and transferred to 45 cm3 of sterile phosphate-buffered saline (pH 7.2) and were shaken vigorously by hand for 1 min to suspend bacteria. Following 30 min sedimentation, the supernatant was serially diluted with sterile phosphate-buffered saline to reach final concentration ranging from 10-1 to 10-3. Collected sample of the seawater was also diluted with sterile phosphate-buffered saline to reach final concentration ranging from 100 to 10-2. Dilutions of sand and seawater samples were filtered through a 0.45 mm pore size, 47 mm diameter membrane filter (Whatman ME 25/31 ST). The filters with collected bacteria were then aseptically transferred to Petri dishes containing 10 cm3 of selective media.

The number of total coliforms was determined using the Endo medium (Biocorp). TC cultures were incubated at 37°C for 48 h and typical red colonies with metallic sheen were counted as the total of coliforms bacteria.

A count of fecal coliforms was determined by the ECD MUG Agar (Fluka). The incubation of inoculations was conducted at the temperature of 44°C for 48 h. After incubation greenish fluorescent colonies indicated cleavage of 4-methylumbelliferone-β-D-glucuronide (MUG) by the β-D-glucuronidase and the released fluorescent MUG compound, which was detected under Wood's lamp (UV light 366 nm); the colonies were counted as FC.

In order to determine the number of fecal streptococci the medium Slanetz-Bartely (Biocorp) was used. After a 48 h incubation at 44°C, red, maroon or pink colonies were counted as FS.

An additional sample of 10 g of sand was weighed (RADWAG WPS 30 S) and dried at 105°C in order to determine the dry weight of sand. All counts were normalized to colony forming units (CFU) per 100 cm3 of seawater or CFU per 100 g of the dry weight of sand.

 

RESULTS

Data presented in Table 1 show that the mean number of total coliform bacteria in seawater samples (583 CFU per 100 cm3) was about two times lower than in wet sand samples (966 CFU per 100 g dry wt of sand) and 3 times lower than in dry sand samples (1807 CFU per 100 g dry wt of sand). Within a year, the highest number of total coliforms bacteria in the seawater occurred in the period from May to July and the lowest in October. In wet sand the highest number of TC was noted in May, while in dry sand from May to August. The lowest number of TC in wet sand was observed in September and October, while in dry sand in September (Fig. 2).

 

Table 1. Abundance of total fecal coliforms (TC), fecal coliforms (FC) and fecal streptococci (FS) in seawater (CFU 100 cm-3) and wet and dry sand (100 g dry weight of sand) (data derived from the pooled data of all months and depths)
Tabla 1. Abundancia de coliformes fecales totales (TC), coliformes fecales (FC) y estreptococos fecales (FS) en agua de mar (CFU 100 cm-3) y arena húmeda y seca (100 g peso seco de arena) (datos derivados de los datos agregados en todos los meses y profundidades)

 

Figure 2. Numbers of total fecal coliforms, fecal coliforms and fecal streptococci in seawater, wet sand and dry sand during the year - long investigation (data derived from the pooled data of all depth)
Figura 2. Números de coliformes totales fecales, coliformes fecales y streptococci fecales en el agua de mar, arena húmeda y seca durante el año de investigación (datos derivados de los datos agregados de todas las profundidades)

 

The mean number of fecal coliforms in dry sand (394 CFU per 100 g dry wt of sand) was 4 times higher than in wet sand (92 CFU per 100 g dry wt of sand) and 3 times higher than in the seawater (142 CFU per 100 cm3) (Table 1). The highest number of FC in the seawater was noted in July and August (Fig. 2), while in April no fecal coliforms were noted. Number of FC in wet sand increased in May and July, while in dry sand in August and September. No presence of fecal coliforms was noted in wet and dry sand in March and April.

The mean of bacterial counts of fecal streptococci in dry sand (1293 CFU per 100 g dry wt of sand) was 6 times higher compared to wet sand (204 CFU per 100 g dry wt of sand) and 9 times higher than in the seawater (150 CFU per 100 cm3) (Table 1). Data presented in Figure 2 show that within a year, we observed the increase in the number of FS in the seawater that started in May and finished in August. In February and April no fecal streptococci were noted in the seawater. In wet and dry sand the highest numbers of FS were recorded in May. In February and March no fecal streptococci were noted in wet sand, while in dry sand in March and April.

Data on number of total coliforms, fecal coliforms and fecal streptococci isolated from the surface (0-5 cm) and subsurface (10-15 cm) sand layers are given in Figure 3. The results of this study showed that all studied fecal bacteria were more numerous in the surface sand layer. Number of these bacteria in the surface layer of wet sand was 2 to 4 times higher than in the subsurface layer. All 3 studied groups of fecal indicator bacteria were 3 to 10 times more abundant in the top layer than in the subsurface layer of dry sand.

 

Figure 3. Fecal bacteria in surface (0-5 cm) and subsurface (10-15 cm) wet and dry sand layer (data derived from the pooled data of all months and sites)
Figura 3. Bacterias fecales en la capa superficial (0-5 cm) y subsuperficial (10-15 cm) de arena húmeda y seca (datos derivados de los datos agregados de todos los meses y sitios)

 

To analyze the relationships among studied bacterial fecal indicators a statistical data evaluation of sand and seawater samples was undertaken and the results are given as the correlation matrix (Table 2). When analyzing wet and dry sand samples together, a very strong correlation (r = 0.86, P < 0.01) was found between total coliform bacteria (TC) in sand and water samples and also total coliforms (TC) and fecal streptococci (FS) in sand samples (r = 0.87, P < 0.01).

 

Table 2. Correlation coefficient fecal indicator bacteria in sand and seawater
Tabla 2. Coeficiente de correlación de indicadores bacterianos fecales en arena y agua de mar

 

Linear regression analysis was also applied to compare relationships between fecal indicators bacteria inhabiting the seawater and sand of the studied beach (Fig. 4). In the seawater, we observed the relation of the number of fecal streptococci (FS) to total coliforms (TC) (R2 = 0.48, P < 0.01), and also of fecal streptococci (FS) to fecal coliforms (FC) (R2 = 0.42, P < 0.01). In sand samples (we analyzed wet and dry sand samples together) we found only statistically significant relation (R2 = 0.76, P < 0.01) of the number of fecal streptococci (FS) to total coliforms (TC).

 

Figure 4. Relationship between mean fecal bacteria densities in seawater and sand of a Beach in Ustka, Poland
Figura 4. Relaciones entre la densidad fecal promedio en el agua de mar y arena en una playa de Ustka, Polonia

 

DISCUSSION

Only recreational coastal waters along marine beaches are systematically sanitary monitored, while the concentration of fecal indicators in the beach sand is not routinely measured despite that the sand beach as a natural filter that may become contaminated with fecal indicator bacteria. These organisms can be transported from the sand to the sea where they may instigate beach advisories (Lee et al. 2006, Bonilla et al. 2007, Yamahara et al. 2009). Law and legislation has emphasised the beach visitors may not use seawater, but would use only the beach sand (Elmanama et al. 2005). They may risk their health due to microbiological contamination in the sand (Olanczuk-Neyman & Jankowska 2001, Vieira et al. 2001, Sato et al. 2005, Heaney et al. 2009).

The year-long study in the Ustka beach demonstrated that fecal bacteria were detected in all study sites (seawater, wet sand, dry sand). Moreover, the number of fecal bacteria was 3-9 times higher in dry sand than in the seawater and 2-6 times higher than in wet sand. Previous studies in marine beaches also showed that the number of fecal bacteria was higher in the sand than in the adjacent water. In 6 public freshwater beaches in St. Clair County, Michigan (USA) fecal bacteria counted in the sand were 3-48 times higher compared to water (Wheeler-Alm et al. 2003), while in a marine beach in Italy, the number of fecal bacteria in the sand was 1 to 30 times higher than in the adjacent seawater (Aulicino et al. 1985). The results of the study in 3 marine beaches of South Florida (USA) were even more striking: the levels of fecal indicator bacteria were on average 100-1000 times greater in the sand relative to seawater (Bonilla et al. 2007). This may be explained by the fact that allochthonous microorganisms inhabiting the beach can survive better in the sand than in the adjacent water (Craig et al. 2002).

According to Lee et al. (2006) and Yamahara et al. (2009) the sand of marine beach represents more stable conditions which are less subject to change than the adjacent seawater. The beach sand may be more conducive to fecal indicator bacteria survival relative to the seawater by reducing the sunlight radiation (Beversdorf et al. 2007, Brownwell et al. 2007), the capability of glycine-betaine accumulation that protects against osmotic stress and lower salinity variation (Heaney et al. 2009). Moreover, the sand is characterized by the significant thermal inertia that effectively reduces a temperature gradient from day to night. This phenomenon secures stable thermal conditions for microorganisms inhabiting the sand (Heaney et al. 2009). The sand also protects against predators (Wheeler-Alm et al. 2003, Lee et al. 2006), and provides colonizable surfaces (Craig et al. 2004, Elmanama et al. 2005). According to Vieira et al. (2001), Kischner et al. (2004) and Whitman et al. (2004) solar radiation, mainly UV light, in combination with salinity is arguably the most potent in the inactivation or killing fecal coliforms and fecal streptococci in seawater. The research of Fujioka et al. (1981) showed that in the absence of sunlight, fecal indicators survive for a few days in seawater samples, whereas in the presence of sunlight, 90% of fecal coliforms and fecal streptococci are inactivated within 30-90 and 60-180 min, respectively. According to Whitman et al. (2004) the process of inactivation or killing fecal bacteria by sunlight in natural waters is rather complex; however, the two major pathways involved in this process appear to be photobiological (DNA damage) and photooxidation (oxidation of cellular components).

Previous studies in marine beaches identified dry sand as the main reservoir of fecal bacteria (Shibata et al. 2004, Sato et al. 2005, Beversdorf et al. 2007, Yamahara et al. 2009). In the studied Ustka beach, the number of fecal bacteria was higher in dry than in wet sand. The results of our study are also consistent with those of Vieira et al. (2001) who found higher amounts of fecal bacteria in dry than in wet sand in 3 marine beaches in Brazil. Similar results were reported by Bonilla et al. (2007) from the Hobie Beach in South Florida, USA. The high number of fecal bacteria in dry sand that it is not under the influence of the tides may indicate that the seawater is not the main source of fecal contamination in this zone of the beach. The statistical analysis in 16 marine beaches of São Paulo State (Brazil) indicated a high correlation between fecal bacteria densities in wet sand and seawater, but not between dry sand and seawater (Sato et al. 2005). According to Haack et al. (2003), Whitman & Nevers (2003), Ishii et al. (2007) and Wright et al. (2009) humans and birds occupying the beach have been main non-point source of fecal bacteria in dry sand. Marine seabirds, for example gulls can excrete more fecal bacteria per day than humans (Jones & White 1984). Thus gulls' fecal droppings are the more prominent source of fecal bacteria in the sand beach (Fogarty et al. 2003, Edge & Hill 2007). Permanent residents of the studied beach are numerous gulls which population grows rapidly in the region of Ustka town every year (Zielinska et al. 2007). Gulls are the most familiar and social birds and quickly adapt to the presence of people (Levesque et al. 1993). They eat not only fish, but to a greater extend use waste and food remaining left by recreational users. Seagulls and other bird type species are attracted by the easy access to food. All of them contribute to the increase contamination of sand by excreting on the beach (Oshiro & Fujioka 1995). Gould & Flechter (1978) determined that the average wet weight of faeces excreted by different gull species ranged from 11.2 to 24.9 g day-1 and one gull could produce between 34 and 62 of fecal droppings in a day. Haack et al. (2003) found that gulls carried a burden of high fecal bacteria in their gastrointestinal tract, with numbers as 1.4 107 of fecal coliforms g-1 and 5.0 107 of fecal streptococci g-1 of faeces. Single gull dropping has been shown to increase the numbers of background streptococci by between 100 and 1000-fold in the 3 m2 area around the dropping (Bonilla et al. 2006). Gull fecal material is considered a threat to human health. The presence of human pathogens in gull faeces such as Salmonella spp., Aeromonas spp., Campylobacter spp., Listeria monocytogenes and Escherichia coli serotype 0157 were documented by Hatch (1996), Levesque et al. (2000) and Fogarty et al. (2003). According to Haack et al. (2003) bird faeces are delivered to the beach via multiple pathways. The movement of people on the beach may contribute to the abundance of indicator bacteria and their distribution in dry sand. In high traffic areas, fecal bacteria can be translocated by people on average 1.6 m in just 4 h (Bonilla et al. 2007). In addition, a study by Alderisio & DeLuca (1999) indicated a fairly stable concentration of fecal bacteria in gull fecal material over 4 seasons during 2 sampling years. Even in non-bathing seasons many visitors of Ustka town, which is a health resort, walking along the beach can spread bird faeces delivered in the sand.

Apart from birds, particularly in summer season, a significant source of fecal bacteria in dry sand of the marine beach is recreational users (Haack et al. 2003, Whitman & Nevers 2003). The same applies to the studied recreational Ustka beach. In summer many people spend a lot of time on the beach dry sand. Bacteria in the skin of recreational users stick to sand or are washed into seawater during sea baths (Craig et al. 2004, Elmir et al. 2007).

In this area there are other serious faecal contamination sources of seawater. The polluted river Slupia with the surface of the river hydrological basin of about 1623 km2 carries wastewater from urban and agriculture area as well as 200,000-300,000 m3 year-1 of natural and anthropogenic sediments into the sea within the area of the studied beach (Zawadzka 1996).

In addition, according to Bonilla et al. (2007) the higher fecal bacteria densities observed in dry sand compared to wet sand may partially also be attributable to lower predation. Predation is a major biotic factor influencing fecal bacteria death rates; it accounted for 47-99% of mortality in water ecosystems (Chigbu et al. 2005). Dry sand contains approximately half of the water content of the intertidal wet sand leading to a reduced water film surrounding sand grains. Macroinvertebrate and larger protozoa, main consumers of bacteria, may not be active in this environment (Bonilla et al. 2007). The second factor contributing to the decrease of the number of faecal bacteria in wet sand is its salinity. The osmotic pressure of salt effectively stops the metabolic processes of bacteria causing the quicker death of cells (Podgórska et al. 2008).

In our study we observed seasonal variation in fecal coliform abundance at the Ustka beach. Generally, during the spring-summer season, the higher abundance of all studied fecal indicator bacteria both in seawater and sand was recorded. Olanczuk-Neyman & Jankowska (2001) in the earlier studies carried out at the Sopot beach (southern Baltic Sea) also reported an increasing trend in the number of fecal bacteria in spring-summer season. Similarly, in Wisconsin beach (Canada) (Zehms et al. 2008), beaches of South Coastal of São Paulo State (Brazil) (Sato et al. 2005) and Duluth Boat Club beach in Minnesota (USA) (Ishii et al. 2007) the number of fecal bacteria was highest from spring to summer months. The high number of fecal bacteria in summer is a potential health risk associated with the exposure of people to the contaminated sand and seawater; particularly children who stay there longer (Sato et al. 2005). This has been observed in the previous study (Whitman & Nevers 2003) and was attributed to the higher survival and perhaps growth rates of fecal bacteria in warmer temperatures. According to Sato et al. (2005) bathers and birds occupying the beach are main potential-point source of fecal indicator bacteria in seawater and the sand of marine beach in summer season.

The results of this study showed that on the Ustka beach all studied fecal bacteria were more numerous in the surface (0-5 cm) than subsurface (10-15 cm) sand layers. Olanczuk-Neyman & Jankowska (2001) in the earlier study carried out on the Sopot beach (southern Baltic Sea) also showed a clear decrease in the number of fecal bacteria with increasing depth. Similarly, in the sand of 6 beaches in St. Clair County, Michigan (USA) the number of fecal coliforms and fecal streptococci in the surface (0-10 cm) layer of the sand was much higher than at the depth of 15-20 cm (Wheeler-Alm et al. 2003). Such distribution results most probably from the fact that the concentrations of organic matter, oxygen and the primary production level of microphytobenthos, which are main stimulators of growth for heterotrophic bacteria, decrease with depth in sand (Mudryk & Podgórska 2007).

In conclusion, the results of this study showed that human pathogenic bacteria of intestinal origin were also present in the sand of marine beach. Therefore, sand of marine and freshwater beaches, which are used for recreational purposes, should be included in sanitary monitoring programs, and this may enhance their effectiveness in human health protection.

 

LITERATURE CITED

Alderisio KA & N DeLuca. 1999. Seasonal enumeration of fecal coliform bacteria from the feces of ring-billed gulls (Larus delawarensis) and Canada geese (Branta canadesis). Applied and Environmental Microbiology 65: 5628-5630.         [ Links ]

Aulicino FA, L Volterra & G Donati. 1985. Faecal contamination of shore-line sands. Bollettino della Società Italiana di Biologia Sperimentale 61: 1469-1476.         [ Links ]

Beversdorf LJ, SM Bornstein-Forst & SL McLellen. 2007. The potential for beach sand to serve as a reservoir for Escherichia coli and the physical influences on cell die-off. Journal of Applied Microbiology 102: 1372-1381.         [ Links ]

Bonilla TD, K Nowosielski, N Esiobu, DS McCorquodale & A Rogerson. 2006. Species assemblages of Enteroccocus indicate potential sources of fecal bacteria at a south Florida recreational beach. Marine Pollution Bulletin 52: 800-815.         [ Links ]

Bonilla TD, K Nowosielski, M Cuveiler, A Hartz, M Green, N Esiobu, DS McCorquodale, JM Fleisher & A Rogerson. 2007. Prevalence and distribution of fecal indicator organisms in South Florida beach sand and preliminary assessment of health effects associated with beach sand exposure. Marine Pollution Bulletin 54: 1472-1482.         [ Links ]

Brownnell MJ, VJ Harwood, RC Kurz, SM McQuaig, J Lukasik & TM Scott. 2007. Confirmation of putative stormwater impact on water quality at a Florida beach by microbial source tracking methods and structure of indicator organism populations. Water Research 41: 3747-3757.         [ Links ]

Byappanahalli MN, RL Whitman, DA Shively, TE Ting, CC Tseng & M Nevers. 2006. Seasonal persistence and population characteristics of Escherichia coli and enterococci in deep backshore sand of two freshwater beaches. Journal of Water and Health 43: 313-320.         [ Links ]

Chigbu P, S Gordon & TR Strange. 2005. Fecal coliform bacteria disappearance rates in a north-central Gulf of Mexico estuary. Estuarine, Coastal and Shelf Science 65: 309-318.         [ Links ]

Colford JM, TJ Wade, KC Schiff, CC Wright, JF Griffiths, SK Sandhu, S Burns, M Sobesz, G Lovelace & SB Weisberg. 2007. Water quality indicators and the risk of illness at beaches with nonpoint sources of fecal contamination. Epidemiology 18: 27-35.         [ Links ]

Craig D, J Fallowield & N Cromar. 2002. Enumeration of faecal coliforms from recreational coastal sites: evaluation of techniques for the separation. Journal of Applied Microbiology 93: 557-565.         [ Links ]

Craig D, J Fallowield & N Cromar. 2004. Use of macrocosms to determine persistence of Escherichia coli in recreational coastal water and sediment and validation with in situ measurements. Journal of Applied Microbiology 96: 922-930.         [ Links ]

Edge TA & S Hill. 2007. Multiple lines of evidence to identify the source of fecal pollution at a freshwater beach in Hamilton Harbour, Lake Ontario. Water Research 41: 3585-3594.         [ Links ]

Elmanama AA, MI Fahd, S Afifi, S Abdallah & S Bahr. 2005. Microbiological beach sand quality in Gaza Strip in comparison to seawater quality. Environmental Research 99: 1-10.         [ Links ]

Elmir SM, ME Wright, A Abdelzaher, HN Solo-Gabriele, LE Fleming, G Miller, M Rybolowik, MT Shih, P Pillai, JE Copoer & EA Quaye. 2007. Quantitative evaluation of bacteria released by bathers in marine water. Water Research 41: 3-10.         [ Links ]

Fogarty LR, SK Haack, MJ Wolcott & RL Whitman. 2003. Abundance and characteristics of the recreational water quality indicator bacteria Escherichia coli and enterococci in gull faeces. Journal of Applied Microbiology 94: 865-878.         [ Links ]

Fujioka R, H Hashimato, E Siwak & R Young. 1981. Effect of sunlight on survival of indicator bacteria in seawater. Applied Environmental Microbiology 41: 690-696.         [ Links ]

Gould DJ & MR Fletcher. 1978. Gull droppings and their effects on water quality. Water Research 12: 665-672.         [ Links ]

Griffith FJ, KC Schiff, GS Lyon & JA Fuhrman. 2010. Microbiological water quality at non-human influenced reference beaches in southern California during wet weather. Marine Pollution Bulletin 60: 500-508.         [ Links ]

Haack SK, LR Fogarty & CG Wright. 2003. Escherichia coli and enterococci at beaches in the Grand Trawerse Bay, Lake Michigan: Sources, characteristics and environmental pathways. Environmental Science and Technology 37: 3275-3282.         [ Links ]

Hartz A, M Cuvelier, K Novosielski, TD Bonilla, M Green, N Esiobu, DS Mc Corquodake & A Rogerson. 2007. Survival potential of Escherichia coli and enterococci in subtropical beach sand: implications for water quality managers. Journal of Environmental Quality 37: 898-905.         [ Links ]

Hatch JJ. 1996. Threat to public health from gulls. International Journal of Environmental Health Research 6: 5-16.         [ Links ]

Heaney CD, E Sams, S Wing, S Marshall, H Brenner, AP Dufour & TJ Wade. 2009. Contact with beach sand among beachgoers and risk of illness. American Journal of Epidemiology 170: 164-172.         [ Links ]

Ishii S, DL Hansen, RE Hicks & MJ Sadowsky. 2007. Beach sand and sediment are temporal sinks and sources of Escherichia coli in Lake Superior. Environmental Science Technology 41: 2203-2209.         [ Links ]

Jones F & WR White. 1984. Health amenity aspects of surface water. Water Pollution Control 83: 215-225.         [ Links ]

Kirschner AK, TC Zechmeister, G Kavka, C Beiwl, A Herzig, RL Mach & AH Farnleitner. 2004. Integral strategy for evaluation of fecal performance in bird - influenced saline inland waters. Applied and Environmental Microbiology 70: 7396-7403.         [ Links ]

Kramarska R, S Uscinowicz, J Zachowicz, P Przezdziecki, J Warzocha, J Netzel & J Janusz. 2003. Identification of submarine deposit drifts to artificial swelling, 55 pp. Department of Marine in Slupia (in Polish). National Geological Institute, Department of Marine Geology, Gdansk.         [ Links ]

Lee CM, TY Lin, C Lin, GA Kohbodi, A Bhatt, R Lee & JA Jay. 2006. Persistence of fecal indicator bacteria in Santa Monica Bay beach sediments. Water Research 40: 2593-2602.         [ Links ]

Levesque BP, P Brousseau, P Simard, E Dewailly, MM Meisels, D Yamasy & J Joly. 1993. Impact of the ring-billed gull (Larus delawarensis) on the microbiological quality of recreational waters. Applied and Environmental Microbiology 59: 1228-1230.         [ Links ]

Levesque BP, P Brousseau, F Bernier, E Dewailly & J Joly. 2000. Study of the bacterial content of ring-billed gull droppings in relation to recreational water quality. Water Research 34: 1089-1096.         [ Links ]

Mudryk Z & B Podgórska. 2007. Abundance and distribution of culturable microorganisms in sandy beaches in south Baltic Sea. Polish Journal of Ecology 55: 221-231         [ Links ]

Olanczuk-Neyman K & K Jankowska. 2001. Bacteriological quality of the sand beach in Sopot (Gdañsk Bay, Southern Baltic). Polish Journal of Environmental Studies 10: 451-455.         [ Links ]

Oshiro R & R Fujioka. 1995. Sand, soil and pigeon droppings: sources of indicator bacteria in the waters of Hanauma Bay, Oahu, Hawaii. Water Science of Technology 31: 251-254.         [ Links ]

Podgórska B, ZJ Mudryk & P Skórczewski. 2008. Abundance and production of bacteria in a marine beach (southern Baltic Sea). Polish Journal of Ecology 56: 405-414.         [ Links ]

Sato MI, MD Bari, C Lamparelli, AC Truzzi, MC Coelho & EM Hachich. 2005. Sanitary quality of sands from marine recreational beaches of São Paulo Brazil. Brazilian Journal of Microbiology 23: 321-326.         [ Links ]

Shibata T, HM Solo-Gabriele, LE Fleming & S Elmir. 2004. Monitoring marine recreational water quality using multiple microbial indicators in an urban tropical environment. Water Research 38: 3119-3131.         [ Links ]

Stewart JR, RJ Gast, RS Fujioka, M Solo-Gabriele, JS Meschke, LA Amaral-Zettker, E del Castillo, MF Polz, TK Collier, MS Strom, D Singigalliano, PD Moeller & AF Holland. 2008. The coastal environment and human health: microbial indicators, pathogens, sentinels and reservoirs. Environmental Health 7: 1-14.         [ Links ]

Vieira RH, DP Rodrigues, EA Menezes, NS Evangelista, EM Reis, M Barreto & FA Goncalves. 2001. Microbial contamination of sand from major beaches in Fortaleza Ceara State, Brazil. Brazilian Journal of Microbiology 32: 77-80.         [ Links ]

Wheeler-Alm WE & J Burke & A Spain. 2003. Fecal indicator bacteria are abundant in wet sand at freshwater beaches. Water Research 37: 3978-3982.         [ Links ]

Whitman RL & MB Nevers. 2003. Foreshore sand a source of Escherichia coli in nearshore water of Lake Michigan beach. Applied and Environmental Microbiology 69: 5555-5562.         [ Links ]

Whitman RL, MB Nevers, GC Korinek & N Byappanahalli. 2004. Solar and temporal effects of Escherichia coli concentration at a Lake Michigan swimming beach. Applied and Environmental Microbiology 70: 4276-4285.         [ Links ]

Wright ME, HM Solo-Gabrieke, S Elmir & LE Fleming. 2009. Microbial load from animal feces at a recreational beach. Marine Pollution Bulletin 58: 1649-1656.         [ Links ]

Yamahara KM, SP Walters & AB Boehem. 2009. Growth of Enterococci in unaltered, unseeded beach sands subjected to tidal wetting. Applied and Environmental Microbiology 75: 1517-1524.         [ Links ]

Zawadzka E. 1996. Litho-morphodynamics in the vicinity of small ports of the Polish Central Coast. In: Taussik J & J Mitchel (eds). Partnership of the coastal management, 353-360. Samara Publ. Limited, Cardigan.         [ Links ]

Zawadzka-Kahlau E. 1999. Trends in South Baltic coast development during the last hundred years. Peribalticum 7: 115-136.         [ Links ]

Zehms TT, CM McDermott & GT Kleinheinz. 2008. Microbial concentrations in sand and their effect on beach water in Door County, Wisconsin. Journal of Great Lakes Research 34: 524-534.         [ Links ]

Zielinska M, P Zielinski, P Kolodziejczyk, P Szewczyk & J Batleja. 2007. Expansion of the Mediterranean Gull Larus melanocephalus in Poland. Journal of Ornithology 148:543-548.         [ Links ]

Received 16 February 2012 and accepted 5 November 2012
Associate Editor: Claudia Bustos D.