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Ecology of the Sontecomapan Lagoon, Veracruz

 | 
Maria Elena Castellanos-Páez
, 
Alfonso Esquivel Herrera
, 
Javier Aldeco-Ramírez
, 
et al.

Organic and inorganic contamination

Evaluation anthropic fecal contamination through enteropathogenic genera identification in Sontecomapan coastal lagoon, Veracruz

Ruth Soto-Castor et Alfonso Esquivel-Herrera

Résumé

Sontecomapan Lagoon is a coastal system located in the Gulf of Mexico which during the late years of the 20th century was equally considered either as a referent of a pristine site or as a man-affected system. Adding to this uncertainty, there are no published references on the microbiological quality of its water. With this purpose, fecal pollution was assessed through the spatial and temporal distributions of total fecal coliforms and enteropathogenic bacteria genera, which were analysed through four surveys (March and September, 2009, January and May, 2010), from ten sampling stations. Total heterotrophic bacteria were simultaneously determined, as well as some physical and chemical variables, and chlorophyll a, to assess the prevailing environmental conditions. Fecal coliform densities surpass the permissible levels and the presence of enteropathogenic genera Salmonella and Shigella poses a further alert. Multivariate analysis (cluster analysis and principal component analysis) highlighted the relation between the abundance and distribution of fecal coliform and enteropathogenic bacteria to the influence of human settlements and livestock husbandry, as well as the lack of correlation between total heterotrophic bacteria and coliform bacteria.

Texte intégral

Introduction

1Coastal lagoons are transitional zones between continent and sea, and they are considered areas of high productivity (Contreras, 1985). One of the major threats to these coastal waters is that they are subject to the impact from the surrounding communities located at their periphery; this way Lagoons suffer the impact of human discharges mainly from domestic waters and fecal waste from livestock (López-Portillo et al., 2017).

2This kind of studies, in the Sontecomapan Lagoon are scarce, even more it has not been emphasized the importance of detecting the enterobacterial genera presence, especially pathogens such as Salmonella and Shigella (Clayton et al., 2016). The genera mentioned cause diseases such as salmonellosis, typhoid fever, bacillary dysentery and other infections acquired through water or shellfish intake, but other, like Klebsiella, also affect the respiratory and urinary tracts, putting human health at risk when in contact with polluted water (Chow et al., 2013). Even though some of these genera may also inhabit in the native fauna of these ecosystems as waterfowl and reptiles, these microorganisms also indicate the presence of ill humans who live close to these ecosystems, (Mather et al., 2016).

3The importance of finding these microorganisms in waterbodies is that edible species are extracted from these systems to be commercialized and consumed locally and regionally, putting human health at risk when organisms such as fish and crustaceans may have fecal bacterial pathogens (Clayton et al., 2016).

4Coliform bacteria have been used for a long time as indicators of fecal contamination (Fecal Indicator Bacteria, FIB) of water and their detection indicates that human or animal excreta have been discharged to urban effluents, or to water discharges from agriculture and from livestock raising activities. Finally, these discharges arrive to coastal lagoons and the sea (Mallin et al., 2000; Sidhu et al., 2012).

5Enterobacteria survival and growth depend on the environmental conditions at the discharge site and on the biotop where they finally arrive; for example, mangroves are rich in organic matter and nutrients that sustain the growth of the native and allochthonous bacterial communities in the lagoon ecosystems, including those of enteric origin (Cho et al., 2010, Stumpf et al., 2010, Vasco et al., 2015).

6Because of this, the purpose of this study is: a) to analyze the temporal and spatial distribution of heterotrophic and coliform bacteria, and the presence of enterobacterial genera of anthropic origin at Sontecomapan, b) to determine the relation of physicochemical and environmental variables with the FIB concentrations.

Material and Methods

Study area and sampling points

7Sontecomapan is a coastal lagoon located at 18º30’ N to 18º34’ N and 94º47’ to 95º11’ W, covering about 891 ha; freshwater inflow comes from three rivers (López-Portillo et al., 2017) (Fig. 1).

Figure 1. Location of the sampling stations at Sontecomapan lagoon.

Figure 1. Location of the sampling stations at Sontecomapan lagoon.

8This lagoon is connected to the sea through a 5.5 m-depth and 137 m-width inlet delimited by a sandy bar known as Barra de Sontecomapan. The lagoon is shallow with a mean depth of 1.67 m (López-Portillo et al., 2017). The mangroves and wetlands bordering this lagoon are part of the wildlife protection zone known as Reserva de la Biosfera de los Tuxtlas (Calva et al., 2005).

9Coastal ecosystems in the Gulf of Mexico, particularly coastal lagoons, are submitted to the influence of three climatic seasons: north wind, dry, and rainy (Contreras, 1985). Annual rainfall ranges between 3000 and 4000 mm. The region is considered as isothermal with maximum temperatures of 26 °C during May and minima of 22 °C in January. Generally, water turbidity is high, with a mean transparency of 0.60 m for the Secchi disk. Water surface temperatures have an average of 24 °C and no vertical thermic difference is noted along the water column. The southern portion of the lagoon is mesohaline (salinity from 5 to 18 PSU), while the central portion is considered as polyhaline (25-30 PSU); the mouth shows euhaline values (30-40 PSU) (Contreras, 1985).

10Ten stations were sampled at subsurface depth of 0.3 m and at 0.3 m above the water-sediment interface (Fig. 1). The choice of the sampling stations was made considering representative locations of the diverse ecological and hydrological features as we as inflow from rivers, streams and the influence of domestic, agricultural or aquaculture discharges (Table 1).

Table 1. Sampling points names, station number and coordinates

Sampling Point

Coordinates

La Boya

N 18°33’02.6”

1

W 94°59’26.8”

El Chancarral

N 18°32’53.2”

2

W 95°00’52”

La Palma

N 18°32’21”

3

W 95°01’02.1”

El Cocal

N 18°32’21”

4

W 95°00’24.8”

Punta Levisa

N 18°32’10”

5

W 95°00’42.3”

El Sabalo

N 18°32’09.8”

6

W 95°00’49.2”

El Real

N 18°33’19.3”

7

W 95°00’51.7”

Rìo Basura

N 18°31’41.3”

8

W 95°02’68”

El Fraile

N 18°30’51.7”

9

W 95°00’39.5”

Costa Norte

N 18°32’49”

10

W 95°01’20.7”

11Sampling was conducted in dry and north wind seasons (March, 2009 and January, 2010, respectively) and in rainy time (September, 2009 and June, 2010), covering the three climatic seasons for this region (Contreras, 1985).

12At each station, one sample of surface and one of bottom water were taken with a Van Dorn bottle. Subsamples were collected into sterile 250 ml flasks, which had been previously cleaned and rinsed with 1 % sodium thiosulfate solution to inhibit residual chlorine. The samples for bacteriological analysis were kept in the dark at 4 °C and processed within 6 hours.

13Physical and chemical data were simultaneously measured at each sampling station, on the four surveys and the results are described later in this volume (Esquivel & Soto).

14For the direct count of total bacteria, subsamples were immediately drawn from the 250 ml flasks into 20 ml sterile amber flasks and preserved with 0.22 µm-filtered formaldehyde to a final concentration of 2 %, and then stored in the dark at 4 °C. Water samples were filtered on black 0.22 µm pore size polycarbonate membranes (25 mm diameter) and then stained with the fluorochrome 4’, 6-diamidine-2-phenylindol (DAPI) for 15 min (Porter & Feig, 1980). Bacteria were counted with epifluorescence microscopy with an Olympus BIMAX50 microscope provided with a 50W mercury lamp and a narrow-band excitation filter (365/366 nm). A minimum of 400 cells was counted in each sample (Kepner & Pratt, 1994).

15Total and fecal (thermotolerant) coliform bacteria and Escherichia coli were estimated by the Most Probable Number (MPN) method in multiple fermentation tubes (Hussong et al., 1981; APHA AWWA & WPCF, 1992). Cellular morphology was described from Gram-stained slides, to confirm the presence of gram-negative bacilli and comma-shaped bacilli. The total coliform bacteria were cultured for 24 hours at 37.0ºC in lactose broth medium and Brilliant Green Bile Lactose broth and the fecal coliform bacteria were cultured for 48 hours in both broths at 44.0 °C. Biochemical identification of enteropathogenic bacteria was carried out based on Farmer et al. (2007). Biochemical confirmation of presumptive isolates of enteropathogenic genera was performed for pure cultures using the bioMérieux API 20E and API 20NE kits (L’ Étoile, France) for biochemical identification of fermenting facultative and non-fermenting Gram-negative strains, respectively. As a further test, cytochrome-oxydase and catalasa were applied on the pure cultures for growth for a period of 16 to 20 hours at 37 °C. The results were run through bioMérieux’s APILab Plus V.3.0 to further identify each isolate.

16Statistical analysis was performed on environmental data after normalization; all data (not averages) were entered into the analysis. Multivariate analysis (cluster analysis and principal component analysis) were applied to data for their clustering and ordination to analyse the association between environmental conditions. Bacterial abundance and distribution data were transformed to z for their cluster analysis (Legendre & Legendre, 1984) based on Euclidean distance and Ward’s aggregation algorithm for clustering by sampling site; values transformed to log10 (X+1) were employed for ordination through principal component analysis in order to analyse the links between environmental conditions (Pielou, 1984). For all these analysis, Statistica for Windows 7 (StatSoft, Tulsa, Ok.) was employed.

Results

Environmental conditions

17During the surveys here considered, the lagoon was characterized by: (i) warm water with a minimum of 24 °C and a maximum of 33 °C, (ii) Secchi disk depth ranged from 0.18 to 2.10 m, (iii) pH from 6.4 to 7.8, and iv) salinity from 0.1 to 36.0 PSU (Esquivel & Soto, this volume). Nitrate and nitrite showed low values for the four surveys; the highest concentrations were detected in September with 10.8 mg l-1 and 0.06 mg l-1, respectively. Ammonia reached its highest concentrations in June, with 3.57 mg l-1. Total phosphorus ranged from undetectable to 2.71 mg l-1 in January, while soluble reactive phosphorus had a minimum of 0.80 mg l-1 in January and a maximum of 26.84 mg l-1 in June. Dissolved oxygen concentrations ranged from 0 mg l-1 in March to a maximum of 9.42 mg l-1 in June, at the onset and end of the dry season, respectively. Chlorophyll a had average values of 0.98 µg L-1 in March 2009, 0.38 µg L-1 in September 2009 and 0.73 µg L-1 in January, 2010.

Total bacteria

18During the period considered, total bacteria densities ranged from 2.4 x 104 (surface, March and September, 2009) to 1.1 x 106 cells mL-1 (bottom, March, 2009). The average values ranged from 6.0 x 104 (September, 2009, surface) to 5.9 x 105 cells mL-1 (June, 2010, bottom).

Coliform

19Total coliform ranged from 3 MPN 100 mL-1 (station 10, Costa Norte in March, 2009) to 1200 MPN 100 mL-1 (at various surface sampling points between 2009 and 2010). Mean total coliform were 298 MPN 100 mL-1 at surface, and 409 MPN 100 mL-1 at bottom water. Total coliform average values ranged from 85 MPN 100 mL-1 (January, 2010) to 611 MPN 100 mL-1 (September, 2009) for surface, and from 67 MPN 100 mL-1 (January, 2010) to 762 MPN 100 mL-1 (March, 2009) for bottom water (Table 2, Figs. 2 and 3).

Table 2. Mean and range for the bacterial population (with units) at the surface level (0.3 m depth) and bottom during the four surveys

Surface

March, 2009

September, 2009

January, 2010

June, 2010

Total coliform MPN 100 mL-1

392 (3-1200)

611 (100-1200)

85 (14-250)

103 (4-800)

Fecal coliform MPN 100 mL-1

646 (26-1200)

534 (42-1200)

455 (25-1200)

30 (3-110)

Total bacteria cells mL-1

4
6.4×10 (2.4×104-1.6×105)

4
6.0×10 (2.4×104-1.6×105)

5
2.0×10 (3.3×104-5.0×105)

5
5.0×10 (8.0×104-9.0×105)

Bottom

March, 2009

September, 2009

January, 2010

June, 2010

Total coliform MPN 100 mL-1

762 (46-1200)

624 (67-1200)

67 (14-175)

18 (4-1000)

Fecal coliform MPN 100 mL-1

590 (33-1200)

336 (21-1200)

352 (30-1200)

207 (7-1000)

Total bacteria cells mL-1

5
4.1×10 (9.5×105-1.1×106)

4
9.6×10 (2.6×104-3.7×105)

5
2.0×10 (4.1×104-4.1×105)

5
5.9×10 (2.6×105-9.0×105)

Figure 2. Variations of the total (TotCol) and fecal coliforms (FecCol) concentrations (left scale) and the total bacteria (TB) concentrations (right scale) at the surface water (0.3 m depth) of each station.

Figure 2. Variations of the total (TotCol) and fecal coliforms (FecCol) concentrations (left scale) and the total bacteria (TB) concentrations (right scale) at the surface water (0.3 m depth) of each station.

Figure 3. Variations of the total (TotCol) and fecal coliforms (FecCol) concentrations (left scale) and the total bacteria (TB) concentrations (right scale) at the bottom level of each station.

Figure 3. Variations of the total (TotCol) and fecal coliforms (FecCol) concentrations (left scale) and the total bacteria (TB) concentrations (right scale) at the bottom level of each station.

20Fecal coliform ranged from 3 MPN 100 mL-1 (station 5, Levisa; June, 2010) to 1200 MPN 100 mL-1 (various surface and bottom water samples, except from June, 2010). Means of fecal coliform were 417 MPN 100 mL-1 at surface and 371 MPN 100 mL-1 at bottom water. Mean of fecal coliforms at surface ranged from 30 MPN 100 mL-1 (June, 2010) to 646 MPN 100 mL-1 (March, 2009) and from 207 MPN 100 mL-1 (June, 2010) to 590 MPN 100 mL-1 (March, 2009) (Table 2, Figs. 2 and 3). A lack of correlation was observed between total bacterial concentrations and coliform, as well as between total and fecal coliform.

Enterobacteriaceae Identification

21The highest number and diversity of enterobacterial isolates from surface and bottom water samples was obtained in January, 2010 while the lowest number and diversity was found in the sampling for June, 2010 (Table 3). Isolates of Enterobacteria genera such as Enterobacter, Klebsiella, Escherichia, Serratia, Citrobacter, and Proteus (some of which are part of coliforms) were obtained in all surveys; they were found in the Basura stream and were found also near the settlements at Chancarral and El Real. The fecal indicator Escherichia was isolated in all the seasons, both in the samples of surface water and bottom water. Salmonella was mainly detected in September and June, corresponding to the rainy season, while the enteropathogenic genus Shigella appeared in all the surveys. It must be emphasized that the latter genus is associated to ill humans, but Salmonella can originate from human or non-human sources. The greater abundance and genera diversity was associated to the sampling points influenced by streams (Basura and La Palma), and shallow areas with contribution from livestock and poultry excreta (El Chancarral and Fraile) and domestic waste (El Real) (Figs. 4 and 5). The highest number of enterobacterial isolates was obtained from the bottom water samples, except for January (Figs. 4 and 5).

Table 3. Number of bacterial isolates by survey, Sontecomapan, Veracruz

March
2009

September
2009

January
2010

June
2010

69

47

92

34

Figure 4. Generic composition of Enterobacteriaceae per sampling point and survey at surface: A. March, 2009 B. September, 2010 C. January, 2010 D. June, 2010

Figure 4. Generic composition of Enterobacteriaceae per sampling point and survey at surface: A. March, 2009 B. September, 2010 C. January, 2010 D. June, 2010

Figure 5. Generic composition of Enterobacteriaceae per sampling point and survey at bottom: A. March, 2009 B. September, 2010 C. January, 2010 D. June, 2010

Figure 5. Generic composition of Enterobacteriaceae per sampling point and survey at bottom: A. March, 2009 B. September, 2010 C. January, 2010 D. June, 2010

22In terms of abundance by survey, the dry and Nortes seasons, showed the highest abundance with 69 and 92 isolates respectively, whereas rainy season surveys, had 47 and 34 bacterial isolates (Table 3). In relation to diversity, surface water samples showed lower genus diversity than bottom water samples. Salmonella and Shigella genera were also present (Figs. 4 and 5).

Multivariate Analysis

23A cluster analysis from abiotic and biotic variables showed two main trends in relation with the station location and the sampling depth. First, no stratification was detected for any sampling point or season. Second, sampling stations differed from the north and eastern portion to those located in the south and western, as shown by the two major clusters. These further were subdivided into lesser subclusters. One of them comprised the sampling stations La Boya (1), Chancarral (2), and El Real (7), situated along the channel connecting to the sea. The second cluster included sampling points Cocal (4), Levisa (5) and Sábalo (6), at the intermediate part of the lagoon. The sampling points at the inner part of the lagoon, Basura (8), Fraile (9) and Costa Norte (10) fell into another cluster. These subclusters are equivalent to the euhaline, polyhaline and mesohaline zones found by Contreras (1985), respectively. The stream at La Palma clustered apart because it is influenced by freshwater (Fig. 6).

Figure 6. Dendrogram of Euclidean distance through Ward’s method showing similarity between sampling stations based on the 11 parameters studied. Samples were noted S and B for surface and bottom, respectively.

Figure 6. Dendrogram of Euclidean distance through Ward’s method showing similarity between sampling stations based on the 11 parameters studied. Samples were noted S and B for surface and bottom, respectively.

24PCA was performed on the independent data sets (11 variables, 10 stations, and 4 months). The first two eigenvalues accounted for 52 % of the total variability. Survey clustering was based on the PCA, and resulted as follows: June, 2010 (early rainy season) was the survey that most differed from the other, with positive values for the first ordination axis. March 2009 and January, 2010 (dry and north wind season) formed a subgroup with negative values for the first and second ordination axes. September, 2009 (full rainy season) had the most negative values for the first ordination axis, but positive for the second (Fig. 7).

Figure 7. Principal component analysis (PCA) of the two first axes based on 11 studied parameters from all samplings. Eigenvalues for each PCA axe are reported. Ordination by parameters and sampling points. Chla chlorophyll a, Fcoli fecal coliform, NH3 Total ammonia, NO2 Nitrite, NO3 nitrate, PO4 soluble reactive phosphorus, PTOT total phosphorus, TB total bacteria, Tcoli total coliform.

Figure 7. Principal component analysis (PCA) of the two first axes based on 11 studied parameters from all samplings. Eigenvalues for each PCA axe are reported. Ordination by parameters and sampling points. Chla chlorophyll a, Fcoli fecal coliform, NH3 Total ammonia, NO2 Nitrite, NO3 nitrate, PO4 soluble reactive phosphorus, PTOT total phosphorus, TB total bacteria, Tcoli total coliform.

25PCA, by variables (Fig. 7), shows that the main ordination axis closely correlates at its positive part with chlorophyll a, and total heterotrophic bacteria and, to a lesser degree, with dissolved oxygen, salinity and reactive soluble phosphorus, which occurred with higher values during the early rainy season of 2010. At the negative part of this axis occurred the variables linked to sanitary indicator bacteria (total coliforms and fecal coliforms); a correlation analysis was run which determined that heterotrophic bacteria densities were directly correlated to chlorophyll a concentration (p<0.001).

26Salinity negatively correlates with the full rainy season of 2009 (September), which presented the lowest salinities. The second ordination axis has nitrate and total ammonia at its positive end and nitrite at the negative. Total coliform correlate to the same rainy season survey of 2009, when they were more abundant, whereas fecal coliform and total phosphorus correlate to the north wind season of 2010 (January) and the dry season of 2009 (March); these last two surveys are located at the negative part of the second ordination axis (Fig. 7).

Discussion

27Even if Sontecomapan is a relatively small coastal lagoon, due to its morphometry it presents a complex behaviour which, in a spatial sense, allows the regionalization that appears in the cluster analysis (Fig. 5). There is another overlaid variation pattern which results from seasonal variation, especially between the dry and rainy seasons. This affects the distribution and survival of native planktonic bacteria, as well allochthonous bacteria, including those of fecal origin.

28Total bacterial counts were lower than would be expected for a tropical coastal lagoon, as they varied between 104 and 106 cells ml-1, values which correspond to oligotrophic tropical waters and lie below the expected range for coastal waters (106 to 107 cells ml-1) (Schut et al., 1997), and especially for surface water (Weise, 2004). At a coastal lagoon, a complex interaction occurs between environmental factors which determine the fate of microbial communities, including their flushing by seaward currents, as occurs in the so-called displacement-dominated lagoons (López-Portillo et al., 2017), which may explain these low bacterial densities (Evanson & Ambrose, 2006; Surbeck et al., 2006; Ulrich et al., 2016).

29Even if total bacterial counts made with direct count (Porter y Feig, 1980) were low, except for surface water during June, 2010; fecal (thermotolerant) coliform bacteria exceeded USA-EPA’s (1988) recommended maximum permissible values for bathing water of 126 NMP 100 mL-1 and of 14 NMP 100 mL-1, with no more than 10 % of the samples exceeding 43 NMP 100 mL-1 for shellfish extraction or harvesting. They also surpassed the maximum allowable value for fecal coliform of 240 NMP 100 mL-1 for services involving direct contact with water according to Mexican legislation, except for surface and bottom water in June, 2010 (NOM-003-SEMARNAT-1997).

30Coliform bacteria have become the standard for fecal pollution assessment because they indicate the health risks associated to food handling, seafood and water (Balière et al., 2016). However, water quality diagnostics are enriched when identification of enterobacterial genera, mainly pathogens such as Salmonella and Shigella, is considered. Enteric bacteria were formerly believed to have a limited ability for surviving outside the digestive tract but, as they have been isolated from environmental samples with relative ease, this implies that they have adapted to outside environments. In the case of E. coli, it has been determined that it can survive in the dark for up to six times more than other microorganisms in river water, which may explain its constant presence in the Sontecomapan water (Avery et al., 2004; Sinton et al., 2007).

31Our study revealed that fecal coliforms were more abundant in March, in what appears to be the marine-influenced part of the lagoon, comprising La Boya (1), Chancarral (2), La Palma (3) and Cocal (4) (Fig. 1), but this could be explained by considering the upstream sources at La Palma which also contributed to increase inorganic nitrogen and phosphorus (Esquivel & Soto, this volume). Total bacteria were less abundant in September, when large rainfall and low-tide resulted in the seaward transport of planktonic bacteria, but total and fecal coliform appeared at high densities, because of rainfall-associated runoff. On other occasions, the highest bacterial counts appeared at the stations that were most protected from current disturbance or at the stations under the influence of streams or rivers inflowing from human settlements (Aslan-Yilmaz et al., 2004; Ahmed et al., 2016). Thus, fecal coliforms were abundant in January at the northern part of the lagoon, comprising the communication mouth to the sea and the channel, while total coliforms were scarce at most sampling stations. The river inputs explained the highest fecal coliform densities reported from La Palma (3) and El Fraile (9) (Fig. 1). This same trend has been described by other works, when the natural inputs of rainwater runoff add to the freshwater plumes incoming from rivers and contribute to fecal contamination, thus temporal and spatial variation should also be considered (Geldreich, 1996; Ulrich et al., 2016). Another enteric bacteria source comes from drainage and runoff that collect debris from farming facilities, impacting the water quality with fecal pollution (Duse et al., 2016; Vasco et al., 2015).

32The present results confirmed that the major contribution of fecal contamination comes from human settlements and farms in the lagoon’s periphery; fecal wastes from poultry, pigs or cattle are discharged mainly at the stations of El Real and Chancarral. This poses a threat due to the improper use of antibiotics, such as automedication or improper livestock husbandry practices which result in bacterial resistance to them. Salmonella has been isolated from animals and agricultural lands of the United Kingdom and the United States, finding multidrug resistance plasmids to different antibiotics (Hancock et al., 2000; Helms et al., 2005; Leekitcharoenphon et al., 2016).

33It should also be mentioned that other natural sources for fecal contamination into the lagoon are waterfowl excreta that reach the coastal environments and arrive to this place to feed, reproduce and nest. The importance of these birds arrival is that some of the enterobacterial genera of the human digestive tract have also been isolated from the intestine of these wild-type birds that defecate in the mangrove. There are reports since the 1950s that Salmonella enterica serovar typhimurium has been isolated from different bird types that inhabit and travel seasonally throughout North America, Asia and Australia, leading to the spread of these microorganisms across all continents (Hernández et al., 2012; Giovannini et al., 2013; Asakawa et al., 2014).

34While the prevailing environmental conditions of the estuarine environment can produce a die-off of coliform bacteria, as would be expected for a good indicator of fecal pollution, there is a continuous input of them. This situation was observed at sampling points such as El Real, Chancarral, and the lagoon mouth, where septic tanks are commonly used, however, because of their improper design or maintenance, they frequently leak or overflow. Several studies have mentioned that another source of fecal contamination besides pluvial runoff water, are dead birds and small mammals which are dragged into water bodies (Ahmed et al., 2008; Simmons et al., 2008).

35The presence of enteropathogenic genera in coastal water bodies, like Sontecomapan, is indicator of their survival in the environment, even if conditions and are not the optimal for their growth. These microorganisms have adapted to changing conditions which have allowed them to survive or even thrive in adverse environments. This has been confirmed by Salmonella enterica and E. coli survival models performed under laboratory conditions where it was found that at least a few cells can survive under desiccating conditions (Koyama et al., 2017).

36Likewise, Shigella, Klebsiella and Enterobacter, which were isolated at some of our collection sites, have been recovered from aquatic environments, soil and wastewater and are therefore able to survive in conditions that require only minimal water and energy sources in natural environments. Their sanitary importance is that they can cause infections in the digestive and urinary tracts and meninges, so that the pollution of aquatic systems by sick humans or animals excreta poses a health risk to whoever comes in contact with polluted water (Abbott, 2007).

37In soil studies, it was found that E. coli developed a mechanism known as soil-persistence that allows it to survive in soil, and this means that this bacteria is highly versatile for metabolizing some substrates at environmental conditions similar to those presented in this work. The ability of E. coli to live and grow for long periods out from its host’s gut poses some doubt concerning its adequacy as a good indicator of water quality. It is believed that the ability of E. coli for surviving stress conditions is due to the regulatory gene’s response Rpo S (Gayán et al., 2016; Somorin et al., 2016).

38Resistance to oxidative stress, osmotic stress and desiccation have also been studied in environmental strains of Salmonella (Shah et al., 2012; Robbe-Saule et al., 2003) and Citrobacter (Dong et al., 2009). In Sontecomapan these genera occurred in the stations Basura, Chancarral, La Boya and Fraile, where desiccative conditions could occur due to their shallow condition.

39The composition of the microbial community is influenced by the environmental changes, mainly at the shallow or circulation-restricted areas of lagoons (Crabill et al., 1999; Conley, 2000; Dorner et al., 2007), where water condition may rapidly deteriorate (Newton & Mudge, 2003). Excreted enteric bacteria are confronted by a highly competitive environment which is less nutrient-rich than the digestive tract of their hosts. This has become a reason why the adaptive mechanisms of these microorganisms may have evolved, enabling their survival when they are out from their normal habitat (Savageau, 1983). Thus, they may survive or even opportunistically proliferate at coastal environments when provided with adequate nutrients. In Sontecomapan these latter come from continuous discharges of domestic, livestock, or agricultural wastewater and waterfowl droppings.

40In addition, the above also reflects that the species that make up bacterial assemblages of enteric origin, colonize coastal aquatic environments by taking advantage of the nutrient richness and other environmental conditions that favour their reproduction and growth. Finally, the presence of bacterial communities of enteric origin in water and sediments is also sustained by their continuous discharge and the persistence of bacterial communities in to this lagoon system (Muhammad et al., 2012).

Conclusions

41Total bacteria densities positively correlated to chlorophyll a concentrations while total and fecal coliform distribution and abundance were related to runoff from the surrounding human settlements. Thus, there was no correlation among total bacteria and coliform.

42Sontecomapan is fecally polluted, as determined from total and fecal coliforms, which surpass maxima permissible values for services involving direct human contact and shellfish harvesting or extraction.

43The highest coliform counts appeared during the rainy season, due to runoff from the upper parts of the catchment basin, with lesser values during the dry season.

44Potentially pathogenic enteric bacteria were detected, such as those from the Salmonella and Shigella genera.

45The presence of human settlements and human-related activities like cattle and poultry husbandry have an important contribution to fecal pollution in Sontecomapan, but wildlife waterfowl and mammals also play a role.

Acknowledgements

46The present research was supported by the project ECOS-ANUIES-CONACYT M10-A01, as part of the CONACYT joint program México-Francia, and the Evaluación diagnóstica de la estructura del circuito microbiano planctónico y de la dinámica hídrica de la laguna de Sontecomapan, Veracruz project (acuerdos del Rector General 12/008) Universidad Autónoma Metropolitana (UAM).

47We acknowledge the comments by anonymous reviewers to our draft paper, for helping improve it.

48IRD’s technician Alain Hervé designed the study area map and located the sampling points on it.

Bibliographie

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Table des illustrations

Titre Figure 1. Location of the sampling stations at Sontecomapan lagoon.
URL http://books.openedition.org/irdeditions/docannexe/image/35559/img-1.jpg
Fichier image/jpeg, 26k
Titre Figure 2. Variations of the total (TotCol) and fecal coliforms (FecCol) concentrations (left scale) and the total bacteria (TB) concentrations (right scale) at the surface water (0.3 m depth) of each station.
URL http://books.openedition.org/irdeditions/docannexe/image/35559/img-2.jpg
Fichier image/jpeg, 49k
Titre Figure 3. Variations of the total (TotCol) and fecal coliforms (FecCol) concentrations (left scale) and the total bacteria (TB) concentrations (right scale) at the bottom level of each station.
URL http://books.openedition.org/irdeditions/docannexe/image/35559/img-3.jpg
Fichier image/jpeg, 56k
Titre Figure 4. Generic composition of Enterobacteriaceae per sampling point and survey at surface: A. March, 2009 B. September, 2010 C. January, 2010 D. June, 2010
URL http://books.openedition.org/irdeditions/docannexe/image/35559/img-4.jpg
Fichier image/jpeg, 32k
Titre Figure 5. Generic composition of Enterobacteriaceae per sampling point and survey at bottom: A. March, 2009 B. September, 2010 C. January, 2010 D. June, 2010
URL http://books.openedition.org/irdeditions/docannexe/image/35559/img-5.jpg
Fichier image/jpeg, 36k
Titre Figure 6. Dendrogram of Euclidean distance through Ward’s method showing similarity between sampling stations based on the 11 parameters studied. Samples were noted S and B for surface and bottom, respectively.
URL http://books.openedition.org/irdeditions/docannexe/image/35559/img-6.jpg
Fichier image/jpeg, 36k
Titre Figure 7. Principal component analysis (PCA) of the two first axes based on 11 studied parameters from all samplings. Eigenvalues for each PCA axe are reported. Ordination by parameters and sampling points. Chla chlorophyll a, Fcoli fecal coliform, NH3 Total ammonia, NO2 Nitrite, NO3 nitrate, PO4 soluble reactive phosphorus, PTOT total phosphorus, TB total bacteria, Tcoli total coliform.
URL http://books.openedition.org/irdeditions/docannexe/image/35559/img-7.jpg
Fichier image/jpeg, 37k

Auteurs

Doctorado en Ciencias Biológicas y de la Salud, Universidad Autónoma Metropolitana. Communication with the autor: 54837000 ext. 3184. Laboratorio de Ecología Microbiana. Departamento de El Hombre y su Ambiente, Ciencias Biológicas y de la Salud, Universidad Autónoma Metropolitana, Unidad Xochimilco. C.P. 04960, CDMX.

Doctorado en Ciencias Biológicas y de la Salud, Universidad Autónoma Metropolitana. Communication with the autor: 54837000 ext. 3184. Laboratorio de Ecología Microbiana. Departamento de El Hombre y su Ambiente, Ciencias Biológicas y de la Salud, Universidad Autónoma Metropolitana, Unidad Xochimilco. C.P. 04960, CDMX.

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