Inventory of benthic marine and estuarine algae and Cyanobacteria for Tabasco , México

Studies of benthic marine and estuarine algae as well as Cyanobacteria are in their early stages in the littoral of the state of Tabasco. Sixty seven taxa of seaweeds are currently known from Tabasco. The inventory of these organisms was made based on samples obtained in six localities, three of them in marine and three in estuarine environments. We found 147 species and subspecific taxa with Rhodophyta having the greatest number with 84, followed by Chlorophyta 44, and finally Phaeophyceae 19. In addition, the 26 species of Cyanobacteria collected are recorded for the first time for the coast of Tabasco since there are no previous reports. The presence of 115 species of benthic marine and estuarine algae is reported for the first time for Tabasco. Most of the new records are Rhodophyta (53.9%), followed by Chlorophyta (29.5%) and Phaeophyceae (16.6%). Of the 115 new records of algae for Tabasco, Gayliella fimbriata and Grateloupia subpectinata are new records also for the Mexican Atlantic. The highest number of species was recorded for Sanchez Magallanes breakwater, while the lowest number of taxa was recorded for Mecoacan Lagoon. According to the Feldmann and Cheney indexes the algal flora of the coast of Tabasco is tropical. The greatest diversity was found during the rainy season.


Introduction
The Gulf of México is characterized by a relatively shallow but well developed continental shelf with an extensive system of generally deep, hard banks of varying origin and composition (Fredericq et al. 2009).In spite of the extension of the Gulf of Mexico coast, in the Mexican portion it has been scarcely studied from the phycological point of view.The phycological literature (Ortega et al. 2001;Wynne 2017) highlights the limited records for the coast of Tabasco.Orozco-Vega & Dreckmann (1995) reported six taxa for the Laguna Mecoacan, an estuarine environment; and Ramirez (1996) recorded 24 species of red algae (Rhodophyta) for the Sanchez-Magallanes breakwater.On the other hand, Dreckmann & De Lara (2000) described the vegetative and reproductive structures of Gracilaria caudata (Rhodophyta) for Laguna Mecoacan.Sentíes & Dreckmann (2013) updated information about the marine and estuarine algae for Tabasco, and recorded 50 taxa of algae for the Tabasco littoral.Recently, Quiroz-González et al. (2017) reported 17 Chlorophyta as new records for this coast.Of the five publications mentioned above, the most complete is that of Senties & Dreckmann (2015), who published an inventory of marine and estuarine algae recorded until 2000 for the coast of Tabasco; also sampled in four localities: Playa El Bellote, Playa El Cangrejo, Laguna Mecoacan and

Study site and collections
The shoreline of the state of Tabasco is between 092˚ 28 'and 094˚ 10' W, and 17˚15' and 18˚ 39' N, located in the southeast meso-region of Mexico, bounded on the north by the Gulf of Mexico (Figure 1); the south by the coastline of Tabasco; to the east northeast by the state of Campeche; and to the west by the state of Veracruz (Hernández-Santana et al., 2008).The Tabasco coastline presents a morphological predominance of low sandy beaches.The coast of Tabasco has a warm humid weather type Am (f): one with a higher annual average temperature of 22 ° C. Rains occur in the summer months and the precipitation of the driest month is less than 60 mm; the percentage of winter rain is higher than 10.2% of the annual total (García y Vidal-Zepeda, 1990a), with minimum extreme values between 20 and 22 ° C in January, and maximum between 30 and 34 ° C in May (García y Vidal-Zepeda, 1990b).Sampling was carried out in the littoral of Tabasco in August and November 2015 and in April and June 2016.The collections were made in the intertidal zone, 0.5 to 1.5 meters deep for sampling sites were chosen by the type of substrate and of access to the localities.A total of 120 samples was collected at six localities: Sanchez Magallanes breakwater (marine environment), La Machona (marine environment), Playa Paraiso breakwater (marine environment), Laguna La Machona, Laguna Mecoacan and Pedro Centla (these three localities of estuarine environment) (Figure 1).Data on the GPS coordinates, type of substrate, depth and date of collection in which organisms were obtained are shown in Table 1.Algae were preserved in a 5% formalin/sea water solution.Small fragments were cut manually with a double-edged blade, and stained with aniline blue and hematoxilin-eosine for anatomical observations and measurements.All specimens of red and brown macroalgae were carefully checked under the microscope for epiphytes.Using a stereoscopic microscope Zeigen HG571405 and an optical microscope OLYMPUS CX3 epiphytic algae were found growing on macroalgae as Gracilaria, Grateloupia, Cladophora and Chnoospora, among others.Thalli were thoroughly reviewed from the base to the apical portion locating filamentous epiphytes and articulated or fleshy macrophytes.After that using a double-edged blade, longitudinal scrapings of 2 cm of each thallus were performed in order to locate microscopic algae (Mateo-Cid et al., 2013).
For the study of descriptive phytogeography, Feldmann (1937) proposed the R / P index (number of Rhodophyta species divided by the number of Phaeophyceae species) useful for classifying the flora of a given region as a function of the latitudinal gradient.Thus, a value of the ratio R / P> 4 is characteristically found in tropical regions, while R / P <2 corresponds with a phycoflora of cool temperate regions.On the other hand, Cheney (1977) included the Chlorophyta (C) based on the one previously mentioned: (R + C) / P and verified that values of the ratio (R + C) / P> 6 are obtained in tropical floras, while those in temperate-cold seas are <3.

New records of algae and cyanobacteria for Tabasco
A total of 173 taxa was identified, 84 of them are Rhodophyta, 44 Chlorophyta, 19 Phaeophyceae as well as 26 Cyanobacteria.The taxa identified from our collections are listed in Table 2 with sampling sites, seasonality, marine or estuarine environment and type of substrate where the organisms were collected, where the reference comes from, either from bibliography or collected by the authors, observations on new records for Tabasco and the Atlantic coast of Mexico and herbarium number.Many of the new algae records located in this study are epiphytes and they are not reported frequently in the floristic lists of Mexican coast of Gulf of Mexico (Ortega et al. 2001, Mateo-Cid et al. 2013, Senties & Dreckmann 2013, Wynne 2017).
Two red algae, Gayliella fimbriata (Setchell & N.L. Gardner) T.O.Cho & S.M. Boo and Grateloupia subpectinata Holmes are new records for the Atlantic coast of Mexico.Twenty six Cyanobacteria, 62 Rhodophyta, 18 Phaeophyceae and 34 Chlorophyta are new records for Tabasco.These new records are indicated in Table 2.The following families were the best represented in number of species in the study area: Rhodomelaceae (14), Ceramiaceae (12), Gracilariaceae (7), Cladophoraceae (19), Bryopsidaceae (8) and Ulvaceae (7).These families collectively include 45.57% of the total floristic diversity registered.The highest species richness was recorded in sampling sites with rocky substrate.The locality with the greatest diversity of species and subspecific taxa corresponds to the Sanchez Magallanes breakwater with 123 species, followed by the Playa Paraíso breakwater with 75, Laguna La Machona 35, La Machona 31, San Pedro Centla 26 and finally Laguna Mecoacan with 20 species (Figure 2).

New records for the Atlantic coast of Mexico
Gayliella fimbriata and Grateloupia subpectinata of the coast of Tabasco, Mexico were recorded for the first time.
Reproductive thalli were not found in our collections.
Comments: A particularly interesting case is the finding of Gayliella fimbriata, because this species was first described by Setchell and Gardner (1924) for the Bay of La Paz (Gulf of California, Mexico) as Ceramium fimbriatum and was subsequently transferred by Cho et al. (2008) to G. fimbriata.The presence of characteristic gland cells on the cortical cells and the dimensions of thalli agree with those recorded in specimens from La Paz, BCS, Mexico (Setchell & Gardner, 1924, Dawson, 1962).This species has been reported from Korea, Vietnam, Japan, China, India, Australia, New Zealand, Hawaii, Mariana Islands, Solomon Islands and Galapagos Islands (Guiry & Guiry, 2017).Therefore this is the first record of Gayliella fimbriata for Tabasco and moreover, for the Atlantic coast of America.
Habit and anatomy: The thallus arising from a discoid holdfast is formed by simple or pinnate erect fronds tapering at the ends, mainly compressed, mucilaginous but firm, reddish to blackish purple, sometimes greenish.Thalli are 2.0-7.0 cm high, simple linear compressed and 375-450 µm diameter; cortex 3-5 layers, the cells moniliform or rounded to stellate in   shape 7-8 µm x 7.5-8.5 µm; medulla filamentous with lax filaments of 3-4 µm in diameter.
Tetrasporophytes and gametophytes isomorphic, the gametophytes dioecious with reproductive structures scattered over the entire thallus except the basal parts.
Comments: Regarding the dimensions of the thallus, tetrasporangia and gonimoblasts show a smaller size than those recorded in specimens from Japan (Faye et al., 2004).Mexican specimens of Grateloupia subpectinata are morphologically similar to G. filicina (J.V. Lamouroux) J. Agardh.Nevertheless, both species have a considerable morphological plasticity (Faye et al., 2004, Verlaque et al., 2005).Compressed and branching Grateloupia species are notoriously difficult to identify due to their morphological similarity and lack of clear-cut diagnostic characters.The characteristics of our specimens are closer to the concept of Grateloupia subpectinata, so it is considered a new record for Tabasco and the Mexican Atlantic.This taxon has been also recorded in the Caribbean Islands (Wynne 2017), Britain, France, Spain and Australia (Guiry & Guiry 2017). Biota Neotrop., 17(4)

Floristic composition
Here we report the presence of 115 previously unreported benthic marine and estuarine algae and 26 Cyanobacteria for the continental coasts of Tabasco, two of them, new records for the Atlantic coast of Mexico.Including the recently published reports of species from Tabasco (Senties & Dreckmann 2013, Quiroz-González et al., 2017), the total number of species increases to 194.This represents an increase of 150% (67) updated from the number published in the recent articles of Senties & Dreckmann (2013) and Quiroz-González et al. (2017), who based their analyses on reports in the literature and recent collections obtained by these authors.When analyzing the different taxonomic groups (Table 2), our survey resulted in a considerable increase in the number of Rhodophyta taxa (53.9%), followed by Chlorophyta (29.5%), and Phaeophyceae (16.6%).
In this study, a total of 26 taxa of Cyanobacteria were found at six localities of Tabasco and constituted 17.67% of the new records.A list of identified species is given in Table 2.There was a dominance of members of the orders Oscillatoriales and Pleurocapsales (27%), and Nostocales (15%), and all 26 taxa were reported for the first time in studies of the Tabasco coast.Species with wide distribution in the study area are Lyngbya confervoides, Calothrix parietina and Scytonematopsis crustacea, all of which have been reported in Campeche and Quintana Roo.With regard to the species of Chroococcales and Pleurocapsales, such as Pseudocapsa maritima, Chroococcus ercegovicii, Aphanocapsa littoralis, all were recorded from one locality, while Entophysalis conferta was present in five of the six study sites, being the most frequent and abundant of all the cyanobacteria recorded in our study.
In the last 50 years, the presence of cyanobacteria in brackishwater systems has been increasingly reported worldwide.Then, a wide diversity of cyanobacteria species can be found in brackish water systems (Lopes & Vasconcelos 2011).In this study, ten species of Cyanobacteria were observed in San Pedro Centla, locality with estuarine environment, while in the Sanchez Magallanes breakwater 16 species were recorded.Finding such a number of species confirms the ability of cyanobacteria to colonize the substrate available, ability for epiphytism, and to form mats in brackish (estuarine) and marine waters.
Most of these organisms requires culture studies and, when possible also the application of molecular-genetic techniques (Bernecker & Wehrtmann 2009).A detailed taxonomic analysis of these taxa will result in higher species numbers for Tabasco.

Type of environment and substrate
According to our study, of the 173 species, 109 develop exclusively in marine environment, 20 in estuarine environment, while 43 were located in both estuarine and marine environments.Most of the Rhodophyta develop in marine rocky areas, whereas members of Chlorophyta are established and developed in both marine and estuarine environments.In the case of brown algae, most of them ( 14) occur in the marine environment.These results agree with those described by McGlathery et al. (2013), who indicated that brown and red algae are almost exclusively marine species and the Chlorophyta can occasionally be abundant in the lower salt marsh zone in estuaries.
In our study, the localities with rocky substrate with marine water influence present high species richness compared with estuarine localities.A total of 89 species was registered in this type of substrate.The rocky substrate is favorable for the development of a great number of marine tropical seaweeds of Ceramiales, Corallinales, Cladophorales and Bryopsidales.On the other hand, the sampling sites with artificial substrate as plastic, net ropes, fishing lines, textiles and concrete debris present lower richness (25); it may be because the artificial substrate limits growth of marine algae and cyanobacteria because they aren't hard and/or stable (Santelices 1977, Garduño-Solórzano et al. 2005, Mateo-Cid et al. 2013).Moreover, our results agree with the statement by Hartog (1967), who indicates that the flora of the brackish water is poor in species in comparison with those of the sea and the fresh water.Most of the marine organisms are stenohaline and are unable to live permanently in water with a higher or lower salt-content than that of the sea.

Epiphytic species
Epiphytes are small size, often microscopic, and their adaptive strategy as epiphytes depends on the permanence of their host and is affected by competition between them for the substrate and light, among other factors.The identification of these species is complicated because their characteristics are difficult to observe.On the other hand, previous works were developed with different objectives, so they have not been similarly inventoried.
Seventy-five epiphytic species (Table 2) were found, 25 of which correspond to Cyanobacteria, 35 to Rhodophyta, six to Phaeophyceae and nine to Chlorophyta.The highest number of epiphytes was observed in the dry season with 45, with a greater number of cyanobacterial species, as well as the families Acrochaetiaceae, Rhodomelaceae and Ceramiaceae, which cover other algae up to almost 90% of their surface.This finding agrees with what is observed in some brown algae and marine phanerogams, in which the level of epiphytism is greater when the surface and biomass of these organisms are larger.This condition is also attributed to the decrease of defense substances against the epiphytes as the host becomes senescent (Ortuño-Aguirre and Riosmena-Rodríguez, 2007).
Most of the epiphytes were frequently found growing on perennial red algae such as Acanthophora, Bryocladia, Gracilaria, and Grateloupia.It has been suggested that host longevity should be long enough to allow these organisms to complete their life cycle and that this might be a likely reason for the absence of epiphytes on annual and ephemeral algae (Santelices, 1977).

Seasonality
Temperature and light determine the latitudinal distribution of seaweeds, and therefore their geographical distribution for they also influence the composition, variation and periodicity of populations at the intertidal and subtidal levels (Santelices, 1977).In our study area summer days are 4 to 5 hours longer that in the winter.Hence, the availability of light for seaweed and estuarine organisms is higher, which influences the species richness of these organisms during the summer (rainy season), with 62 Rhodophyta (49.2%), 15 Phaeophyceae (11.9%), 28 Chlorophyta (22.2%) and 21 Cyanobacteria (16.68%).The lowest specific richness occurred in winter rains ("nortes" in which the rain is greater than 10.2% and temperature values between 20 and 22 ° C) with 29 Rhodophyta (46.77%), 1 Phaeophyceae (1.62%), 19 Chlorophyta (30.65%), and 13 Cyanobacteria (20.96%).Finally, during the dry season 41 Rhodophyta (49.4%), 11 Phaeophyceae (13.3%), 24 Chlorophyta (28.9%), and 7 Cyanobacteria (8.4%) occurred (Figure 4) for our results are similar to those reported in previous studies in the Mexican Atlantic where mentioned that the species richness of algae is higher in the rainy season (Ortega et al., 2001, Callejas-Jimenez et al, 2005, Mateo-Cid et al., 2013).
In the rocky zone of the Sanchez Magallanes breakwater and Playa Paraiso breakwater numerous species of the families Corallinaceae, Rhodomelaceae, Ectocarpaceae, Dictyotaceae and Ulvaceae occurred.Rhodophyta dominates in number, with 60 in Sánchez Magallanes and 36 in Playa Paraíso.In the dry and rainy seasons Ulva fasciata, U. rigida, Cladophora vagabunda and Bryopsis pennata are common; while Asteronema breviarticulatum and Ectocarpus siliculosus are the most common in the rainy season.It is evident that in the estuarine areas the smallest number of species is presented, the Laguna Mecoacan having the lowest diversity with only 10 Rhodophyta, 7 Chlorophyta and 3 Cyanobacteria.

Biogeography
The results of the present study were analyzed applying the Feldmann and the Cheney indexes and compared with findings by Mateo-Cid & Mendoza-González (2007) for Cozumel island; Mendoza-González et al. (2007) of Mujeres Island, Dreckmann et al. (1996) for Puerto Morelos, Huerta-Múzquiz et al. (1987), Ortegón-Aznar et al. (2001, 2009) and Sánchez-Molina et al. (2007) for the coast of Yucatán and Mateo-Cid et al. (2013) for the coast of Campeche.Table 3 shows the data obtained applying the Feldmann and Cheney indexes to the five regions mentioned; the phycoflora of the study area is similar to that of the coast of the state of Quintana Roo, with a value close to that obtained for the Cozumel and Mujeres Islands, both distinctly Caribbean localities.
The indexes used indicate that the marine and estuarine algae of the coast of Tabasco have a predominantly tropical distribution, with tropical elements such as Melanothamnus ferulaceus, Hypnea musciformis, Jania adhaerens, Gracilaria flabelliformis, Gracilariopsis longissima, Dictyopteris delicatula, Dictyota crenulata, Chnoospora minima, Chaetomorpha antennina, Ulva rigida and Cladophora flexuosa, among others.The phycoflora of the coast of Tabasco conforms to the pattern found in all coastlines of the states of the Gulf of Mexico (Ortega et al. 2001, Mateo-Cid et al., 2013).

Figure 1 .
Figure 1.Map of the study area and sampling stations.

Figure 2 .
Figure 2. Number of species per division per locality

Figure 4 .
Figure 4. Number of species per division per season

Table 1 .
Location of sampling sites, substrate, environment, depth and collection dates.

Table 2 .
Marine and estuarine algae and Cyanobacteria of the coast of Tabasco (The abbreviations are explained at the end of the table).

Table 3 .
Feldmann and Cheney indexes for some marine and estuarine environments of the Gulf of Mexico and Mexican Caribbean coast.