Introduction

1The phytoplankton of the Sontecomapan lagoon has been studied by Suchil (1990), who carried out a seasonal sampling of communities and reported a succession of diatom and dinoflagellates blooms. Guerra-Martínez (1996) studied the variations in nano and microplankton biomass at the lagoon mouth in 1992 and 1993; Meave del Castillo & Lara-Villa (1997) made an inventory of planktonic diatoms and Figueroa-Torres et al. (2009) made another one on the thecate dinoflagellates from the lagoon. Camacho et al. (1994) studying the circadian rhythms of phytoplankton in October 1993, recorded 90 taxa of which Skeletonema subsalsum was the dominant throughout the cycle. Muciño-Márquez et al. (2011) studied phytoplankton populations in October, 1999 and reported 179 species, from which Fragilaria exigua, F. tenuicollis, F. ulna var ulna, Prorocentrum gracile and Scrippsiella trochoidea were the dominant ones. Both studies agreed that diatoms and dinoflagellates were the most abundant and frequent groups in their samples. On the other hand, Muciño-Márquez et al. (2012), at the same period, recorded 27 red tide-forming species in this lagoon. Specific taxonomic aspects of some species have been studied by others investigators in this lagoon; Aké-Castillo et al. (1995) reported morphological variations of some species from the Skeletonema genus (S. subsalsum, S. pseudocostatum and S. costatum) while Aké-Castillo et al. (2000, 2004) reported species from the Chaetoceros genus (Chaetoceros subtilis var abnormis f. abnormis, Chaetoceros subtilis var abnormis f. simplex). Aké-Castillo & Vázquez-Hurtado (2011) described the presence of Peridinium quinquecorne var trispiniferum and Aké-Castillo (2015) reported the Thalassiosira cedarkeyensis species. In summary, according to the different studies, a very great variability in composition and abundance of phytoplankton species has been observed at different sampling stations and seasons at Sontecomapan Lagoon with no clear distribution patterns.

2Therefore, this work is a contribution to the phytoplankton studies of the Sontecomapan Lagoon by developing an up-to-date list of species with new sampling observations at rainy and dry seasons. Also, this work is a plea for a constant monitoring of the phytoplankton in the lagoon in order to analyze time-changes in the species’ composition and detect the eventual presence of toxic species in the ecosystem to prevent damage to human health.

Materials and Methods

3The Sontecomapan Lagoon is a tropical coastal ecosystem characterized by three zones according to the horizontal salinity gradients: fresh, brackish and marine waters; with two-layer flows and vertical mixtures, associated with the climatic conditions of the region (Lankford, 1977). The average depth is 1.5 meter. The combination of physical and chemical factors leads to the formation of zones with different microenvironmental conditions of location and variable dimensions, which favor the differential development of phytoplankton species. Eight sampling stations were set up along the lagoon: La Boya, Río La Palma, El Real, Estero El Fraile, Punta Levisa, El Chancarral, Río Sábalo and Río Basura (Fig. 1). Sampling was performed in June, 2015 (rainy season) and February, 2016 (dry season).

Figure 1. Location of the Sontecomapan Lagoon and sampling stations

(Modified from Image @DogotalGlobe, Image@2016TerraMetrics)

4Sixteen phytoplankton samples were collected at subsurface level of the water column using a Van Dorn bottle and were placed in 500 ml glass bottles preserved with acetate-lugol at 1 %. To perform the counts, samples were homogenized and placed in one-milliliter chambers to be checked under a Zeiss Axiovert 135 inverted microscope, by triplicate. For taxonomic determination, the keys and descriptions by Taylor (1976), Dodge (1982), Balech (1988), Fukuyo et al. (1990), Licea et al. (1995), Bravo (2004), Okolodkov (2010), Gómez (2010, 2013) and García–Mendoza et al. (2016) among others, were consulted. Nomenclature was updated based on the work of Guiry & Guiry (2017).

5Salinity was measured with an Atago SMill-E refractometer series 0183181, pH with an Orion pH meter 250A series 017210; depth and transparency with a Secchi disk, water temperature with a cuvette thermometer (0-100 ºC ± 1 ºC) and the dissolved oxygen concentration was calculated according to Winkler’s technique (Strickland & Parsons, 1972).

6A cluster analysis was performed using the Statistica 8 software, for the environmental conditions of the lagoon.

Results

Physical and chemical factors

7During the rainy season, water depth was greater in stations Canal el Real, Río Sábalo, El Chancarral and La Boya with values of 230, 200, 105 and 100 cm respectively, compared to the dry season, which was shallower, with depths of 73, 180, 44 and 15 cm. Spatially, the deepest stations were recorded far from the mouth at Río Basura and Río Sábalo with values of 320 and 200 respectively in rainfall and 340 and 180 cm in dry. It is clear that the rains and the continental water contributions have a great influence on the depth increase throughout the system (Fig. 2A).

8Transparency was generally high in the two sampling periods, with the exception of Río Basura where transparency was 85 cm in the rainy season and 90 cm in the dry season (Fig. 2B).

9The water temperature ranged between 25 and 33.5 ºC and was higher in the rainy season, where the highest value was obtained in El Fraile (33.5 °C) and the minimum in Río La Palma (25.9 ºC). In the dry season, it varied very little: from 25 to 27°C at the different sampling sites (Fig. 2C).

10As for pH, it remained close to neutrality in both seasons (Fig. 2D); in the rainy season the maximum value was 7.9 at El Real and the minimum at Río Sábalo with a 6.0 value. In the dry season, Río Sábalo showed the maximum value (7.65) and Río La Palma the minimum (6.7). Río Sábalo, El Fraile and La Boya presented the highest pH values in the dry season and the lowest in the rainy season.

11Concentrations of dissolved oxygen showed a spatial variation in the rainy season with highest values at El Chancarral (11.6 mg/L) and Río La Palma (8.8 mg/L) and lowest values at La Boya and Río Sábalo (3.3 mg/L both). In the dry season, values were more homogeneous and varied between 7.8 mg/L at El Chancarral and 5.3 mg/L at Punta Levisa (Fig. 2E).

12Salinity presented great fluctuations, from 0 to 20 psu (Fig. 2F). During the rainy season, maxima of 18 and 19 psu were observed at La Boya and El Real, near the mouth of lagoon, and a minimum of 0 psu in Río La Palma and Río Basura, which are further away from the lagoon’s mouth. It is worth noting that in this season (although not shown in the figures) salinity of the bottom water at El Chancarral and El Real showed values of 35 and 34 psu respectively, forming a wedge-like halocline. In the dry season the highest salinity (20 psu) was recorded at Río Sábalo, although this station is distant from the mouth of the lagoon, whereas the lowest (3 psu) was recorded at Río Basura.

Figure 2. Environmental variables registered in the Sontecomapan Lagoon, Veracruz in rainy season (June, 2015) and dry season (February, 2016). A) depth, B) transparency, C) temperature, D) pH, E) dissolved oxygen and F) salinity.

13The cluster analyses based on physical and chemical data (Fig. 3A-B) established clusters (corresponding to geographic zones) at a link distance of 50. The rainy season was more heterogeneous with four clusters, while the dry season formed three. In the dendrogram corresponding to the rainy season (Fig. 3A), the Río Sábalo and the Canal El Real sampling stations were separated in spite of having the highest values of depth and transparency, salinity, pH and temperature. Probably the morphology of the basins was the main factor since Río Sábalo is more isolated from the zone under tidal influence and therefore, with more stagnant waters, while El Real is under oceanic coastal waters influence and high hydrodynamic conditions. Río Basura that has the lowest salinity formed the third zone and all other sampling stations the fourth zone. In the dry season, Río Basura also formed a single cluster characterized by the lowest salinity, as well as Río Sábalo characterized by the highest. The third cluster grouped the rest of the sampling stations with intermediate salinities. Apparently, the other factors were less important than salinity in this season. However, we can point that at both seasons Río Sábalo, which correspond to the more confined zone, clearly distinguished from all the other stations.

Figure 3 A-B. Dendrograms of Sontecomapan Lagoon, Veracruz, based on physical and chemical data: A) rainy season (June, 2016) and B) dry season (February, 2016)

Phytoplankton

14From literature revision and this study, a list of 357 species was generated for the lagoon (Table 1), from which 241 (67.8 %) were Diatoms, 72 (20.16 %) Dinoflagellates, 13 (3.64 %) Chlorophytes, 11 (3.08 %) Euglenophytes, 16 (4.20 %) Cyanoprokariotes, 2 (0.56 %) Raphydophyceae and 2 (0.56 %) Silicoflagellates.

15We observed that 46 (12.88 %) from the species registered in the general list, are potentially red tide forming (Table 2), and are mainly represented by Dinoflagellates with 20 species (43.48 %) and Diatoms with 19 (41.30 %).

16Among them, 12 species are toxic and five affect humans: Pseudo-nitzschia pungens, Pseudo-nitzschia pungens var atlántica and Pseudo-nitzschia seriata diatoms, which produces domoic acid that causes amnesic poisoning by consumption of contaminated shellfish, Dinophysis caudata dinoflagellate that causes diarrhea and Cyanoprocariota Lyngbya majuscula that produces dermatitis and respiratory diseases.

17Five other species affect the marine fauna: dinoflagellates Gonyaulax spinifera, producer of yessotoxin that can kill fish and invertebrates, Phalacroma rotundatum that may cause problems to salmon in captivity, Prorocentrum gracile that causes fish mortality, Prorocentrum micans that produces verupine (hepatoxin) toxin affecting clams and shellfish, and Tripos furca which may cause great mortality of tuna in captivity. Likewise, the Cyanoprokariota Anabaenopsis circularis has been reported as toxic, but not enough information is available, as well as the Raphydophycea Olisthodiscus luteus, which seems to cause red blood cells lysis.

18From the water samples analyzed in this study, 102 phytoplankton species (Table 1, Plates 1 to 3) were recorded, of which 61 are reported for the first time in the lagoon. Among these 102 species, 69 (67.64 %) belong to the group of diatoms, 17 (16.67 %) to Dinoflagellates, 10 (9.80 %) to Cyanoprokaryotes, 4 (3.93 %) to Euglenophytes and 2 (1.96 %) to Chlorophytes. It was detected that 17 of these species are potentially red tide forming, eight of them being Diatoms, six Dinoflagellates and three Cyanoprokariotes. Only two are toxic for humans: Dinophysis caudata dinoflagellate, that causes diarrhea from contaminated shellfishes consumption, and cyanoprocariota Lyngbya majuscula, which may cause dermatitis and respiratory irritation.

19Fourty two (42) species were collected in the rainy season and 65 in the dry season (Fig. 4A); 7 species were common to both seasons.

20In the dry season, La Boya had the highest richness with 31 species, followed by Río Basura with 29 and El Fraile with 27. In the rainy season, the greatest species richness was registered at Punta Levisa with 18 and Río Sábalo with 14. It is noteworthy that at this season, only two species were registered at El Chancarral.

21Phytoplankton abundance reached values up to 300 x 10⁴ cells/l (Fig. 4B), but mats of the cyanoprokaryote Merismopedia convoluta were also observed in the dry season at El Fraile sampling station with 1600 x 10⁴ cells/l; this value was discarded in the graph (Fig. 4B) because it gives the impression of a massive bloom. However, this species is very small (3-5 μm in diameter), hardly perceptible in site and sample (Plate 3, Fig. 24), considering that most of the phytoplankton organisms measure more than 50 µm, which is 15 times greater than M. convoluta, and with biovolumes 3,000-fold higher.

Figure 4 A-B. Phytoplankton species richness and abundance in Sontecomapan Lagoon, Veracruz, in the rainy (June, 2015) and dry (February, 2016) seasons

Table 1. Phytoplankton of the Sontecomapan Lagoon, Veracruz, Mexico

22In the rainy season, due to their abundance, only two species dominated: the Melosira nummuloides diatom with 21 x10⁴ cells/l at Punta Levisa and the euglenophyte Trachelomonas volvocina with 23 x10⁴ cells/l, at Río Sábalo. In contrast, in the dry season, high abundances of diatoms were observed: Eunotia sp. with 87 x10⁴ cells/l at Río Basura and 4 x10⁴ cells/l at Río La Palma, Melosira moniliformis was frequent in all sampling stations and reaching up to 28 x10⁴ cells/l, Gomphonema parvulum with a high abundance of 26 x 10⁴ cells/l present only at Río Basura. At this latter station, Nitzschia macilenta was observed with 21 x 10⁴ cells/l, although it was also present in seven of the eight sampling stations. Among the dinoflagellates, only Tripos hircus can be highlighted, as it was present in seven of the eight sampling stations, reaching its maximum density of 20 x10⁴ cells/l at Río Sábalo. The cyanoprokaryote Oscillatoria af. limosa showed values of 10.2 x10⁵ cells/l at La Boya, 61 x10⁴ cells/l at El Real, 81 x10⁴ cells/l at Punta Levisa and 27 x10⁴ cells/l at El Chancarral sampling stations. Lyngbya majuscula reached 35 x10⁴ cells/l at Estero El Fraile, Limnoraphis hieronymusii 29 x10⁴ cells/l only at Río Sábalo, and, as already mentioned, Merismopedia convoluta reached a very high density of 1600 x10⁴ cells/l only at El Fraile.

23The cyanoprokaryote Oscillatoria af. limosa showed values of 10.2 x10⁵ cells/l at La Boya, 61 x10⁴ cells/l at El Real, 81 x10⁴ cells/l at Punta Levisa and 27 x10⁴ cells/l at El Chancarral sampling stations. Lyngbya majuscula reached 35 x10⁴ cells/l at Estero El Fraile, Limnoraphis hieronymusii 29 x10⁴ cells/l only at Río Sábalo, and as already mentioned, Merismopedia convoluta reached a very high density of 1600 x10⁴ cells/l only at El Fraile.

Discussion

24It was observed that depth varied little in the sampling stations between the two periods, except at El Real which was far deeper in the rainy season (near 230 cm) than in the dry one (73 cm), probably due to erosion caused by currents. The rest of the sampling stations were shallow, reaching only a few centimeters deep, comparable to the mean depth of Mexican lagoons (150 cm; Lankford, 1977).

25The temperatures recorded in our study (25 to 33.5 ºC) were higher than those reported by Lankford (1977) and García-Cubas & Reguero (1995), with values close to 24 ºC. Likewise, we recorded the highest temperatures in the rainy season, whereas Morán (1994) reported highest values in dry season.

26The highest salinities found in dry season (20 psu) were similar to those previously reported by Morán (1994). At both seasons, the lowest values (0-7 psu) were observed closed to river outlet (La Palma and Basura rivers) and the highest (18-19 psu) in Arroyo la Boya near the mouth of the lagoon. In Río Sábalo salinity fluctuated from 14 to 20 psu, probably due to water stagnation and evaporation, and the low contribution of fresh water from the river, coinciding with that reported by Lankford (1977) and Muciño-Márquez et al. (2012). In this regard, García-Cubas & Reguero (1995) point out that the lagoon is predominantly mesohaline, with frequent fluctuations of 5 to 18 psu.

27The lagoon has a pH close to neutrality (from 6.7 to 7.9) and is rather well oxygenated with concentration showing greater fluctuations in the rainy season (3.3. mg/L to 11.6 mg/L) than in the dry season (5.3 mg/L to 7.8 mg/L), remaining within the appropriate intervals for aquatic life. These values coincide with those reported by Carbajal (2009) for this lagoon, and by Contreras & Warner (2004), Contreras et al. (2005) and López Ortega et al. (2012), for other lagoons in the State of Veracruz.

28We did not measure nutrients during this study, but according to Castro-Gutiérrez et al. (1985), nutrients are not usually limiting for the development of phytoplankton in the lagoon due to river inputs and contributions of matter from the adjacent vegetation together with the recycling mechanisms and processes.

29According to Lankford (1977), Castro-Gutiérrez et al. (1985), Martínez (1987), Morán (1994), Figueroa-Torres et al. (2009), Muciño-Márquez et al. (2011a, 2012) and Esquivel & Soto-Castor (this issue), the Sontecomapan lagoon presents three zones, based on morphology, and on gradients of salinity and nutrient concentration. The first is oligohaline with high fresh water influence and highest nutrient level. The second, in the central channel, is considered as a transition zone between mesohaline and polyhaline water, with the lowest nutrient values and greater salinity variations. The third zone, euhaline, corresponds to the lagoon’s mouth. This zone behaves as an area of water masses exchange with the coastal zone and over time, recycling of nutrients has been observed at different scales as a consequence of the process of water mass regeneration and population succession. These processes are directly influenced by climatic seasonal changes, hydrometeorological conditions, and circadian and tidal rhythms, all of them widely recognized as important in the study of phytoplankton (Castro-Gutierrez et al., 1985; Guerra-Martínez, 1996; Figueroa-Torres et al., 2009 & Muciño-Márquez et al., 2011 a, b and 2012), and were also probably important drivers for the variability observed in this study.

30The dendrogram showed a spatial arrangement in the dry season very similar to the salinity gradients described above, with three different areas clearly related to salinity. However, in the rainy season our results suggest differences also linked to morphological characteristics of the sites. At this period, the Río Sábalo was separated from El Real probably due to its location in a confined area with little current and evaporation processes, maintaining high salinity values while El Real, located near the mouth of the lagoon, had high seawater influence linked to tidal effect (Muciño-Márquez, 2011a, b). Río Basura, farther from the mouth of the lagoon, has higher hydrodynamic and greater fresh water influence than El Sábalo.

31From the samples analyzed in this work, a total of 102 phytoplankton species were recorded. The predominance of diatoms and dinoflagellates agrees with that reported by Muciño-Márquez, (2011a, b). The highest abundance occurred in February, 2017, corresponding to the dry season, in agreement with Suchil (1990) who points out that the dry months produce stability and adequate conditions for the best development of phytoplankton.

32Of the species identified, 61 are new records for the lagoon, this suggests that species richness may be underestimated, possibly due to the presence of very diverse microenvironmental conditions and to the constant introduction and species exchange of continental and marine origin by the water currents.

33Additionally, in the dry season, it was observed that the richness and abundance of species were very variable throughout stations and sampling sites, with importance of freshwater species in the rainy season and of potentially toxic or harmful algae of marine lineage, aspects that were repeatedly observed in previous studies (Guerra-Martínez & Lara-Villa, 1996; Figueroa-Torres et al., 2009).

34The most frequent and abundant species was Tripos hircus, especially in the dry season, with a maximum density of 20 x 10⁴ cells/l. Guerra-Martínez and Lara-Villa (1996) recorded high densities of this species in the lagoon, at salinities of 13-35 psu and temperatures of 30 to 34 °C. The decrease of its population was associated with the increase of freshwater inputs in the system. Figueroa-Torres (1990), Zamudio-Reséndiz (1998) and Okolodkov (2010), among others, have observed that this species is common in the waters of the Gulf of Mexico, and López (1980) considers it as an indicator of nutrient-rich and warm water.

35Within the species recorded, 17 are potentially harmful, and 2 may affect human health: the Dinophysis caudata dinoflagellate that may cause diarrhea through consumption of contaminated shellfish and, the cyanoprocariota Lyngbya majuscula that may cause dermatitis and respiratory irritation.

36By combining our results with historical data, we could establish a current register of 357 phytoplankton species for the Sontecomapan Lagoon. This inventory is dominated by diatoms and dinoflagellates, characteristic of brackish and marine environments, but also includes freshwater microalgae such as chlorophytes and euglenofites showing the polyhaline nature of the lagoon ecosystem.

37Among this list 46 species formed algal blooms, and 12 of them are potentially toxic, five species affect humans and five more affect marine fauna.

Table 2. Species of phytoplankton of the Sontecomapan Lagoon, Veracruz, that can form blooms.

38It is worth noting that most of the toxic species were present in the dry season, so special attention should be paid to their presence at this season. It is not possible to rule out the possibility that the above-mentioned species may be present again and in higher concentrations. Besides new harmful and toxic species may also develop because of accelerated processes of eutrophication of anthropic origin in the last years in the coastal lagoons, which can affect economic production, human health and marine biota.

Conclusions

39The Sontecomapan lagoon is an ecosystem with marked hydrodynamic processes at different times of the year. Salinity appears as a determinant factor, which confers a polyhaline character to the system, forming three characteristic zones: the first with strong influence of fresh water, the second brackish and the third with more marine influence.

40Other physical and chemical factors such as pH, temperature and dissolved oxygen generate particular microenvironmental conditions that drive the distribution and abundance of phytoplankton species, in addition to which the intrinsic characteristics of the species must be considered in order to tolerate certain environmental conditions. However, there are few studies on this subject and so far, no clear behavioral patterns can be established.

41From this study, a list of 102 species was obtained, with 61 new records for the area, with only two species toxic to man and none for aquatic fauna. Combining this list with previous historical data, we could establish a current list of 357 phytoplankton species for the lagoon, of which 46 are potentially harmful or toxic.

42Due to the importance of this resource, it is necessary to continue sampling and monitoring the phytoplankton of the Sontecomapan Lagoon, since the harmful and toxic species can develop and reach alarming densities at any time, emphasizing the dry season, when more problematic species are present. It is also important to consider that the accelerated process of anthropic origin eutrophication that occurred in the last years in the Mexican coastal lagoons may affect the economic production, human health and marine biota.

Acknowledgements

43This study was supported by the 2002-39634-F/A-1 project CONACYT, the Mobility ECOS-ANUIES-CONACYT Program (189448) and the Universidad Autónoma Metropolitana, Unidad Xochimilco. The authors thank Lic. Suny Ramírez Figueroa for her support in the manuscript review.