Abstract

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.

Keywords:
Tabasco; Mexico; new records; marine; estuarine; algae; Cyanobacteria

Resumo

Estudos sobre algas marinhas, estuarinas e cianobactérias para o litoral do estado de Tabasco encontram-se apenas nos estágios iniciais. Neste estudo, um inventário desses organismos foi feito com base em amostras obtidas em seis localidades, três delas marinhas e três em ambientes estuarinos. Os resultados indicaram a presença de 147 táxons, com Rhodophyta apresentando maior diversidade (84), seguido de Chlorophyta (44) e, finalmente, Phaeophyceae (19). Além disso, 26 espécies de Cyanobacteria são registradas pela primeira vez para a costa de Tabasco. A presença de 115 espécies de algas marinhas e estuarinas bentônicas é relatada peloa primeira vez para Tabasco. A maioria dos novos registros são de Rhodophyta (53.9%), seguido por Chlorophyta (25.9%), e Phaeophyceae (16.6%). Dos 115 novos registros de algas para Tabasco, Gayliella fimbriata e Grateloupia subpectinata são novos registros para a costa atlântica do México. O maior número de espécies foi localizado no paredão de Sanchez Magallanes, enquanto o menos número de táxons foi localizado na Lagoa Mecoacán. De acordo com os índices de Feldmann e Cheney, a flora de algas da costa de Tabasco é tropical, e a maior diversidade foi encontrada durante a estação chuvosa.

Palavras-chave:
Tabasco; México; registros novos; marinhos; estuarinos; algas; cianobactérias

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. 2009FREDERICQ, S., GURGEL, C.F.D., NORRIS, J.N., EARLE, S., MATEO-CID, L.E., MENDOZA-GONZÁLEZ, A.C. & SUÁREZ, A.M. 2009. Seaweeds (Rhodophyta, Chlorophyta and Phaeophyceae) of the Gulf of Mexico. In: Gulf of Mexico, origins Waters and Biota: Biodiversity. (D.L. Felder & D.A. Camp, eds.). Texas A&M University Press, College Station, Texas. v. 1, p. 45-87.). 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. 2001ORTEGA, M. M., GODÍNEZ-ORTEGA, J. L. & GARDUÑO-SOLÓRZANO, G. 2001. Catálogo de algas bénticas de las costas mexicanas del Golfo de México y Mar Caribe. Comisión Nacional para el Estudio de la Biodiversidad y Universidad Nacional Autónoma de México. México, D.F., México.; Wynne 2017WYNNE, M. J. 2017. A checklist of benthic marine algae of the tropical and subtropical western Atlantic: fourth revision. Nova Hedwigia Beihefte 145: 1-202.) highlights the limited records for the coast of Tabasco. Orozco-Vega & Dreckmann (1995)OROZCO-VEGA, H. & DRECKMANN, K.M. 1995. Macroalgas estuarinas del litoral Mexicano del Golfo de México. Cryptogamie Algol 16: 189-198. reported six taxa for the Laguna Mecoacan, an estuarine environment; and Ramirez (1996)RAMÍREZ, L.A. 1996. Estudio preliminar de las algas rojas (Rhodophyta) del litoral del estado de Tabasco, México. Tesis Profesional, Universidad Nacional Autónoma de México, Iztacala. Tlalnepantla, Estado México, México. 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)QUIROZ-GONZÁLEZ, N., LEÓN-ÁLVAREZ, D. & RIVAS-ACUÑA, M.G. 2017. Nuevos registros de algas verdes marinas (Ulvophyceae) para Tabasco, México. Acta Bot Mex 118: 121-138. DOI: http://dx.doi.org/10.21829/abm118. 2017.1204
http://dx.doi.org/10.21829/abm118. 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 Sánchez Magallanes breakwater, recording 50 taxa of algae, of which Rhodophyta had the highest number (38), followed by Phaeophyceae (7) and Chlorophyta (5). Quiroz-González et al (2017)QUIROZ-GONZÁLEZ, N., LEÓN-ÁLVAREZ, D. & RIVAS-ACUÑA, M.G. 2017. Nuevos registros de algas verdes marinas (Ulvophyceae) para Tabasco, México. Acta Bot Mex 118: 121-138. DOI: http://dx.doi.org/10.21829/abm118. 2017.1204
http://dx.doi.org/10.21829/abm118. 2017.... carried out several collections in seven localities: Playa Miramar, Pico de Oro, Playa Paraiso, Poblado Chiltepec, Playa de Dos Bocas, Playa Las Brisas and Sanchez Magallanes breakwater; their study was based exclusively on Chlorophyta and the authors reported 17 new records of this group for the coast of Tabasco. In conclusion, it is evident that the length of the coast of Tabasco has not been equally inventoried and there are even portions which have not been studied at all, and the different groups of marine and estuarine algae have not been equally studied either.

Collectively, our knowledge about the cyanobacteria of the Tabasco coast is also limited. Cyanobacteria have been omitted in most studies conducted on the Mexican Atlantic benthic algae. Among the few reports that have been published is that of Mateo-Cid et al. (2013)MATEO-CID, L.E., MENDOZA-GONZÁLEZ, A.C. AVILA-ORTIZ, A.G. & DÍAZ-MARTÍNEZ, S. 2013. Algas marinas bentónicas del litoral de Campeche, México. Acta Bot Mex 104: 53-92..

The aims of this study are to provide an updated revision of the diversity and distribution of the benthic marine and estuarine algae and Cyanobacteria of three new localities of the coast of Tabasco (San Pedro Centla, Laguna La Machona, La Machona), besides Sánchez Magallanes breakwater, Playa Paraíso breakwater and Laguna Mecoacan. We include records of new algae and cyanobacteria for Tabasco, as well as data about their distribution and temporal variation during the dry, rainy summer and rainy winter seasons (nortes). Using the Feldmann and Cheney indexes, the phycoflora of the coast of Tabasco will be classified as a function of the latitudinal gradient, and thus establish the basis for future taxonomic, ecological and biogeographic studies.

Materials and methods

1. 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., 2008HERNÁNDEZ-SANTANA, J.R., ORTIZ-PÉREZ, M.A, MÉNDEZ LINARES, A.P. & GAMA CAMPILLO, L. 2008. Morfodinámica de la línea de costa del estado de Tabasco, México: tendencias desde la segunda mitad del siglo XX hasta el presente. Investigaciones Geográficas, Boletín del Instituto de Geografía UNAM 65: 7-21.). 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, 1990aGARCÍA, E. & VIDAL-ZEPEDA R. 1990a. Temperatura media. Atlas Nacional de México, Hoja IV.4.4, Instituto de Geografía, UNAM, México.), with minimum extreme values between 20 and 22 ° C in January, and maximum between 30 and 34 ° C in May (García y Vidal-Zepeda, 1990bGARCÍA, E. & VIDAL-ZEPEDA R. 1990b. Temperaturas extremas, Atlas Nacional de México, Hoja IV.4.5, Instituto de Geografía, UNAM, México.). 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., 2013MATEO-CID, L.E., MENDOZA-GONZÁLEZ, A.C. AVILA-ORTIZ, A.G. & DÍAZ-MARTÍNEZ, S. 2013. Algas marinas bentónicas del litoral de Campeche, México. Acta Bot Mex 104: 53-92.).

Figure 1
Map of the study area and sampling stations.

Semi-permanent slides were prepared using corn syrup/water 1:1 with a trace of phenol added to prevent fungal growth. The identification at the specific level was based mainly on Taylor (1960)TAYLOR, W. R. 1960. Marine algae of the eastern tropical and subtropical coasts of the America. University of Michigan Press. Ann Arbor., Schneider & Searles (1991)SCHNEIDER, C. W. & SEARLES, R. B. 1991. Seaweeds of the southeastern United States. Cape Hatteras to Cape Cañaveral. Duke University Press. Durham., Littler & Littler (2000)LITTLER, D.S. & LITTLER, M.M. 2000. Caribbean reef plants. An identification guide to the reef plants of the Caribbean, Bahamas, Florida and Gulf of Mexico. Offshore Graphics. Washington., Cho et al. (2008)CHO, T. O., BOO, S. M., HOMMERSAND, M.H., MAGGS, C.A., MCIVOR, L. & FREDERICQ, S. 2008. Gayliella gen. nov. in the tribe Ceramieae (Ceramiaceae, Rhodophyta) based on molecular and morphological evidence. J Phycol. 44(3): 721-738., Dawes & Mathieson (2008)DAWES, C. J. & MATHIESON, A.C. 2008. The seaweeds of Florida. University Press of Florida. Gainesville. and Won et al. (2009)WON, B.Y., CHO, T.O. & FREDERICQ, S. 2009. Morphological and molecular characterization of species of the genus Centroceras (Ceramiaceae, Ceramiales), including two new species. J Phycol 45: 227-250.. For the determination of Cyanobacteria Gomont (1892)GOMONT, M. 1892 '1893'. Monographie des Oscillariées (Nostocacées Homocystées). Deuxième partie. – Lyngbyées. Ann Sci Nat Bot, Ser 7 16: 91-264., Anagnostidis & Komárek (1988)ANAGNOSTIDIS, K. & KOMÁREK, J. 1988. Modern approach to the classification system of Cyanophytes. 3. Oscillatoriales. Arch Hydrobiol Suppl. 80: 327-472., Komárek & Anagnostidis (1995)KOMÁREK, J. & ANAGNOSTIDIS, K. 1995. Nomenclatural novelties in chroococcalean cyanoprokaryotes. Preslia 67: 15-23., and Komárek et al. (2014)KOMÁREK, J., KASTOVSKY, J., MARES, J. & JOHANSEN, J.R. 2014. Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach. Preslia 86: 295-335. were used. The sequence of the floristic list follows the order proposed by Komárek (2010)KOMÁREK, J. 2010. Recent changes (2008) in cyanobacteria taxonomy based on a combination of molecular background with phenotype and ecological consequences (genus and species concept). Hydrobiologia 639: 245-259. for Cyanobacteria, Wynne (2017)WYNNE, M. J. 2017. A checklist of benthic marine algae of the tropical and subtropical western Atlantic: fourth revision. Nova Hedwigia Beihefte 145: 1-202. and Guiry & Guiry (2017)GUIRY, M. D. & GUIRY, G.M. 2017. World-wide electronic Publication. National University of Ireland. Galway, Ireland. http://www.algaebase.org. (last access in 25/03/2017).
http://www.algaebase.org... for red, brown and green algae. Most of the material analyzed is deposited and available for study in the phycological section of “Herbario Escuela Nacional de Ciencias Biológicas at the Instituto Politécnico Nacional, Mexico”.

For the study of descriptive phytogeography, Feldmann (1937)FELDMANN, J. 1937. Recherches sur la végétation marine de la Méditerranée. La Côte des Albères. Rev Algol 10: 1-339. 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)CHENEY, D. P. 1977. A new improved ratio for comparing seaweed floras. J Phycol. 13(suppl.): 1-13. 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.

Results

1. 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. 2001ORTEGA, M. M., GODÍNEZ-ORTEGA, J. L. & GARDUÑO-SOLÓRZANO, G. 2001. Catálogo de algas bénticas de las costas mexicanas del Golfo de México y Mar Caribe. Comisión Nacional para el Estudio de la Biodiversidad y Universidad Nacional Autónoma de México. México, D.F., México., Mateo-Cid et al. 2013MATEO-CID, L.E., MENDOZA-GONZÁLEZ, A.C. AVILA-ORTIZ, A.G. & DÍAZ-MARTÍNEZ, S. 2013. Algas marinas bentónicas del litoral de Campeche, México. Acta Bot Mex 104: 53-92., Senties & Dreckmann 2013SENTIES, A. & DRECKMANN, K.M. 2013. Lista actualizada de las macroalgas de Tabasco, México. Acta Bot Ven 36 (2): 109-117., Wynne 2017WYNNE, M. J. 2017. A checklist of benthic marine algae of the tropical and subtropical western Atlantic: fourth revision. Nova Hedwigia Beihefte 145: 1-202.).

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).

Figure 2
Number of species per division per locality

Species and subspecific taxa such as Jania ungulata f. brevior Yendo, Centroceras gasparrinii (Meneghini) Kützing, Spyridia clavata Kützing, Polysiphonia scopolorum var. villum (J. Agardh) Hollenberg, Peyssonnelia armorica (P.L. Crouan & H.M. Crouan) Weber-van Bosse, Hecatonema floridanum (W.R. Taylor) W.R. Taylor, Herponema tortugense (W.R. Taylor) W.R. Taylor, Rosenvingea orientalis (J. Agardh) Børgesen, Blidingia minima (Nägeli ex Kützing) Kylin, Cladophora crispula Vickers and Pseudobryopsis blomquistii Diaz-Piferrer are considered unusual because few records are in the floristic lists of the Mexican coast of the Gulf of Mexico (Ortega et al. 2001ORTEGA, M. M., GODÍNEZ-ORTEGA, J. L. & GARDUÑO-SOLÓRZANO, G. 2001. Catálogo de algas bénticas de las costas mexicanas del Golfo de México y Mar Caribe. Comisión Nacional para el Estudio de la Biodiversidad y Universidad Nacional Autónoma de México. México, D.F., México., Mateo-Cid et al. 2013MATEO-CID, L.E., MENDOZA-GONZÁLEZ, A.C. AVILA-ORTIZ, A.G. & DÍAZ-MARTÍNEZ, S. 2013. Algas marinas bentónicas del litoral de Campeche, México. Acta Bot Mex 104: 53-92., Senties & Dreckmann 2013SENTIES, A. & DRECKMANN, K.M. 2013. Lista actualizada de las macroalgas de Tabasco, México. Acta Bot Ven 36 (2): 109-117., Wynne 2017WYNNE, M. J. 2017. A checklist of benthic marine algae of the tropical and subtropical western Atlantic: fourth revision. Nova Hedwigia Beihefte 145: 1-202.).

Thirty of the 67 species previously recorded for Tabasco (Orozco-Vega & Dreckmann 1995OROZCO-VEGA, H. & DRECKMANN, K.M. 1995. Macroalgas estuarinas del litoral Mexicano del Golfo de México. Cryptogamie Algol 16: 189-198., Ramirez 1996RAMÍREZ, L.A. 1996. Estudio preliminar de las algas rojas (Rhodophyta) del litoral del estado de Tabasco, México. Tesis Profesional, Universidad Nacional Autónoma de México, Iztacala. Tlalnepantla, Estado México, México., Dreckmann & De Lara-Isassi 2000DRECKMANN, K.M. & DE LARA-ISASSI, G. 2000. Gracilaria caudata J. Agardh (Gracilariaceae, Rhodophyta) en el Atlántico mexicano. Hidrobiológica 10: 125-130., Senties & Dreckmann 2013SENTIES, A. & DRECKMANN, K.M. 2013. Lista actualizada de las macroalgas de Tabasco, México. Acta Bot Ven 36 (2): 109-117., Quiroz-González et al., 2017QUIROZ-GONZÁLEZ, N., LEÓN-ÁLVAREZ, D. & RIVAS-ACUÑA, M.G. 2017. Nuevos registros de algas verdes marinas (Ulvophyceae) para Tabasco, México. Acta Bot Mex 118: 121-138. DOI: http://dx.doi.org/10.21829/abm118. 2017.1204
http://dx.doi.org/10.21829/abm118. 2017.... ) were found in this study. The other 115 species (table 2) are considered new records for Tabasco.

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.

Description

Gayliella fimbriata (Setchell & N.L. Gardner) T.O. Cho & S.M. Boo (Figures 3a-d)

Figure 3
Gayliella fimbriata: Sánchez Magallanes (ENCB 22091). 3a. General appearance of the filamentous thallus growing on Spyridia sp (arrowhead). Scale 200 µm. 3b: Base of the thallus on the host (white arrowhead). Note rhizoid (arrow), and the prominent gland cells (black arrowhead) on the cortical bands. Scale 135 µm. 3c: Detail of verticilar arrangement of gland cells (arrowheads). Scale 25µm. 3d: Detail of an apical branch without forcipates apices. Note the apical cell (arrow) and gland cells (arrowheads). Scale 20 µm. 3e. Grateloupia subpectinata: Sanchez Magallanes (ENCB 22031), a: tetrasporangial thallus. Scale 1.6 cm. 3f: G. subpectinata: Sanchez Magallanes (ENCB 22016), Female thallus. Scale 1.8 cm. 3g: Cross-section through a blade showing cortex (arrow) and developing medulla. (Arrowhead). Scale 150 µm. 3h: Cross-section through a blade showing an immature tetrasporangium (arrowhead) and a mature, cruciately divided tetrasporangium. (Arrow) Scale 95 µm. 3i: Close-up of mature gonimoblast (arrow). Scale 80 µm. 3j: Cross-section through a blade showing the gonimoblasts (arrow) borne on an expanded fusion cell. Note the elongated ampullar filaments (arrowhead). Scale 60 µm.

Type locality: Eureka, near La Paz, Lower California Mexico (Setchell & Gardner 1924SETCHELL, W.A. & GARDNER, N.L. 1924. New marine algae from the Gulf of California. Proc Calif Acad Sci Series 4 12: 695-949, 77 plates.: 777).

Basionym: Ceramium fimbriatum Setchell & N.L. Gardner 1924

Representative specimens examined: Sánchez Magallanes (Mendoza González & García López, 26.viii.2015, ENCB 22091, Vegetative).

Habit and anatomy: Thalli are 0.5–1.0 cm high, consisting of prostrate axes giving rise to erect axes (Figure 2). Erect axes bear forcipate incurved and complanate apical regions, main filaments 85-95 µm diameter at the nodes. Axial cells are spherical to cylindrical. The acropetal corticating filaments are 3–4 cells long, while the basipetal ones are 2–3 cells long. Branches are regularly alternate. Gland cells usually develop from cortical cells of acropetally and rarely basipetally corticating filaments, becoming strongly protruding, and are clavate, 60-65 µm x 30-34 µm.

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)SETCHELL, W.A. & GARDNER, N.L. 1924. New marine algae from the Gulf of California. Proc Calif Acad Sci Series 4 12: 695-949, 77 plates. for the Bay of La Paz (Gulf of California, Mexico) as Ceramium fimbriatum and was subsequently transferred by Cho et al. (2008)CHO, T. O., BOO, S. M., HOMMERSAND, M.H., MAGGS, C.A., MCIVOR, L. & FREDERICQ, S. 2008. Gayliella gen. nov. in the tribe Ceramieae (Ceramiaceae, Rhodophyta) based on molecular and morphological evidence. J Phycol. 44(3): 721-738. 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, 1924SETCHELL, W.A. & GARDNER, N.L. 1924. New marine algae from the Gulf of California. Proc Calif Acad Sci Series 4 12: 695-949, 77 plates., 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, 2017GUIRY, M. D. & GUIRY, G.M. 2017. World-wide electronic Publication. National University of Ireland. Galway, Ireland. http://www.algaebase.org. (last access in 25/03/2017).
http://www.algaebase.org... ). Therefore this is the first record of Gayliella fimbriata for Tabasco and moreover, for the Atlantic coast of America.

Grateloupia subpectinata Holmes (Figures 3 d-j)

Type locality: Japan.

Heterotypic synonyms:

Grateloupia luxurians (A. Gepp & E.S. Gepp) R.J. Wilkes, L.M. McIvor & Guiry 2005WILKES, R.J., MCIVOR, L.M. & GUIRY, M.D. 2005. Using rbcL sequence data to reassess the taxonomic position of some Grateloupia and Dermocorynus species (Halymeniaceae, Rhodophyta) from the north-eastern Atlantic. Eur J Phycol 40: 53-60.: 58

Grateloupia filicina var. luxuriansA. Gepp & E.S. Gepp 1906GEPP, A. & GEPP, E.S. 1906. Some marine algae from New South Wales. J Bot 44: 249-261.: 259

Representative specimens examined: Sánchez Magallanes Breakwater (Mateo Cid, Mendoza González & Valencia Torres, 10.iv.2016, ENCB 22996, female thalli and tetrasporangial thalli); Laguna La Machona (Mateo Cid & Mendoza González, 10.iv.2016, ENCB 22006, female).

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.

Tetrasporangia initiated from inner cortical cells, cruciately divided when mature, 14-15 µm wide x 29-30 µm long. Carposporangial ampullae not found; gonimoblasts 60-80 µm immersed inside the medulla and surrounded by branched ampullar filaments and a network of secondary medullary filaments.

Comments: Regarding the dimensions of the thallus, tetrasporangia and gonimoblasts show a smaller size than those recorded in specimens from Japan (Faye et al., 2004FAYE E.J., WANG, H.W., KAWAGUCHI, S., SHIMADA, S. & MASUDA, M. 2004. Reinstatement of Grateloupia subpectinata (Rhodophyta, Halymeniaceae) based on morphology and rbcL sequences. Phycol Res 52:59–67). 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., 2004FAYE E.J., WANG, H.W., KAWAGUCHI, S., SHIMADA, S. & MASUDA, M. 2004. Reinstatement of Grateloupia subpectinata (Rhodophyta, Halymeniaceae) based on morphology and rbcL sequences. Phycol Res 52:59–67, Verlaque et al., 2005VERLAQUE, M., BRANNOCK, P.M., KOMATSU, T., VILLALARD-BOHNSACK, M. & MARSTON, M. 2005. The genus Grateloupia C. Agardh (Halymeniaceae, Rhodophyta) in the Thau Lagoon (France, Mediterranean): a case study of marine plurispecific introductions. Phycologia 44 (5): 477-496.). 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 2017WYNNE, M. J. 2017. A checklist of benthic marine algae of the tropical and subtropical western Atlantic: fourth revision. Nova Hedwigia Beihefte 145: 1-202.), Britain, France, Spain and Australia (Guiry & Guiry 2017GUIRY, M. D. & GUIRY, G.M. 2017. World-wide electronic Publication. National University of Ireland. Galway, Ireland. http://www.algaebase.org. (last access in 25/03/2017).
http://www.algaebase.org... ).

Discussion

1. 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 2013SENTIES, A. & DRECKMANN, K.M. 2013. Lista actualizada de las macroalgas de Tabasco, México. Acta Bot Ven 36 (2): 109-117., Quiroz-González et al., 2017QUIROZ-GONZÁLEZ, N., LEÓN-ÁLVAREZ, D. & RIVAS-ACUÑA, M.G. 2017. Nuevos registros de algas verdes marinas (Ulvophyceae) para Tabasco, México. Acta Bot Mex 118: 121-138. DOI: http://dx.doi.org/10.21829/abm118. 2017.1204
http://dx.doi.org/10.21829/abm118. 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)SENTIES, A. & DRECKMANN, K.M. 2013. Lista actualizada de las macroalgas de Tabasco, México. Acta Bot Ven 36 (2): 109-117. and Quiroz-González et al. (2017)QUIROZ-GONZÁLEZ, N., LEÓN-ÁLVAREZ, D. & RIVAS-ACUÑA, M.G. 2017. Nuevos registros de algas verdes marinas (Ulvophyceae) para Tabasco, México. Acta Bot Mex 118: 121-138. DOI: http://dx.doi.org/10.21829/abm118. 2017.1204
http://dx.doi.org/10.21829/abm118. 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%).

Among the new records we can highlight: Acrochaetium sagreanum, A. microscopicum, Antithamnionella boergesenii, An. elegans, Heterosiphonia crispella, Gayliella mazoyerae, G. fimbriata, Peyssonnelia armorica, Asterocladon rhodochortonoides, Hecatonema floridanum, Herponema tortugense, Phaeophila dendroides, Ulvella lens, Ul. scutata, and Ul. viridis. Epiphytes are a very important group in the algal flora, especially in Tabasco, whose coast has many floodplains, extensive sandy beaches, coastal lagoons, breakwaters, and very exposed rocky coasts, lacking of algae.

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 brackish-water systems has been increasingly reported worldwide. Then, a wide diversity of cyanobacteria species can be found in brackish water systems (Lopes & Vasconcelos 2011LOPES, V.R. & VASCONCELOS, M.V. 2011. Planktonic and benthic cyanobacteria of European brackish waters: a perspective on estuaries and brackish seas. Eur J Phycol 46:3, 292-304.). 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 2009BERNECKER, A. & WEHRTMANN, I.S. 2009. New records of benthic marine algae and Cyanobacteria for Costa Rica, and a comparison with other Central American countries. Helgoland Mar. Res. 63:219–229.). A detailed taxonomic analysis of these taxa will result in higher species numbers for Tabasco.

2. 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)MCGLATHERY, K.J., SUNDBACK.K. & FONG, P. 2013. Estuarine benthic algae. In Estuarine Ecology (J. Day Jr, B.C. Crump, W.M. Kemp & A. Yañez-Arancibia, eds.). New Jersey: A John Wiley & Sons, Inc., Publication. New Jersey. p. 235-264., 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 1977SANTELICES, B. 1977. Ecología de algas marinas bentónicas. Efectos de factores ambientales. Santiago de Chile: Pontificia Universidad Católica de Chile., Garduño-Solórzano et al. 2005GARDUÑO-SOLÓRZANO G., GODÍNEZ-ORTEGA, J. & ORTEGA, M. 2005. Distribución geográfica y afinidad por el sustrato de las algas verdes (Chlorophyceae) bentónicas de las costas mexicanas del Golfo de México y Mar Caribe. Bol Soc Bot Mex 76: 61-78., Mateo-Cid et al. 2013MATEO-CID, L.E., MENDOZA-GONZÁLEZ, A.C. AVILA-ORTIZ, A.G. & DÍAZ-MARTÍNEZ, S. 2013. Algas marinas bentónicas del litoral de Campeche, México. Acta Bot Mex 104: 53-92.). Moreover, our results agree with the statement by Hartog (1967)HARTOG, C. 1967. Brackish water as an environment for Algae. Blumea 15: 31-43., 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.

3. 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, 2007ORTUÑO-AGUIRRE, C. & RIOSMENA-RODRÍGUEZ, R. 2007. Dinámica en el epifitismo de Padina concrescens (Dictyotales, Phaeophyta) en el sureste de la Península de Baja California, México. Cien Mar 33(3): 311-317.).

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, 1977SANTELICES, B. 1977. Ecología de algas marinas bentónicas. Efectos de factores ambientales. Santiago de Chile: Pontificia Universidad Católica de Chile.).

4. 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, 1977SANTELICES, B. 1977. Ecología de algas marinas bentónicas. Efectos de factores ambientales. Santiago de Chile: Pontificia Universidad Católica de Chile.). 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., 2001ORTEGA, M. M., GODÍNEZ-ORTEGA, J. L. & GARDUÑO-SOLÓRZANO, G. 2001. Catálogo de algas bénticas de las costas mexicanas del Golfo de México y Mar Caribe. Comisión Nacional para el Estudio de la Biodiversidad y Universidad Nacional Autónoma de México. México, D.F., México., Callejas-Jimenez et al, 2005CALLEJAS-JIMÉNEZ, M. E., SENTÍES, A. & DRECKMANN, K.M. 2005. Macroalgas de Puerto Real, Faro Santa Rosalía y Playa Preciosa, Campeche, México, con algunas consideraciones florísticas y ecológicas para el estado. Hidrobiológica 15 (1): 89-96., Mateo-Cid et al., 2013MATEO-CID, L.E., MENDOZA-GONZÁLEZ, A.C. AVILA-ORTIZ, A.G. & DÍAZ-MARTÍNEZ, S. 2013. Algas marinas bentónicas del litoral de Campeche, México. Acta Bot Mex 104: 53-92.).

Figure 4
Number of species per division per season

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.

5. 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)MATEO-CID, L.E. & MENDOZA-GONZÁLEZ, A.C. 2007. Flora ficológica: Diversidad, importancia económica y conservación. In Biodiversidad acuática de la Isla Cozumel (L. Mejía-Ortiz, ed.) Distrito Federal: Plaza Valdés. p. 81-113. for Cozumel island; Mendoza-González et al. (2007)MENDOZA-GONZÁLEZ, A. C., MATEO-CID, L. E. & SEARLES, R.B. 2007. Yucatán seaweeds from the offshore waters of Isla Mujeres, Quintana Roo, México. Bot Mar 50: 280-287. of Mujeres Island, Dreckmann et al. (1996)DRECKMANN, K. M., STOUT, I. & SENTÍES, A. 1996. Lista actualizada de las algas marinas bentónicas de Puerto Morelos, Quintana Roo, Caribe mexicano. Polibotánica 3: 1-17. for Puerto Morelos, Huerta-Múzquiz et al. (1987)HUERTA-MÚZQUIZ, L., MENDOZA-GONZÁLEZ, A.C. & MATEO-CID, L.E. 1987. Avance sobre un estudio de las algas marinas de la Península de Yucatán. Phytologia 62: 23-53., Ortegón-Aznar et al. (2001ORTEGÓN-AZNAR, I., GONZÁLEZ-GONZÁLEZ, J. & SENTÍES, A. 2001. Estudio ficoflorístico de la laguna de Río Lagartos, Yucatán, México. Hidrobiológica 11(2): 97-104., 2009ORTEGÓN-AZNAR, I., SÁNCHEZ-MOLINA, I. & CASANOVA-CETZ, R.A. 2009. The distribution of marine algae in a coastal lagoon, northern Yucatan Peninsula, Mexico. Neotrop Biol Conserv 4(2): 99-105.) and Sánchez-Molina et al. (2007)SÁNCHEZ-MOLINA, I., GONZÁLEZ-CEBALLOS, J., ZETINA-MOGUEL, C. & CASANOVA-CETZ, R. 2007. Análisis de la biodiversidad de algas marinas situadas entre Uaymitún y Chuburná, Yucatán. Ingeniería 11(1): 43-51. for the coast of Yucatán and Mateo-Cid et al. (2013)MATEO-CID, L.E., MENDOZA-GONZÁLEZ, A.C. AVILA-ORTIZ, A.G. & DÍAZ-MARTÍNEZ, S. 2013. Algas marinas bentónicas del litoral de Campeche, México. Acta Bot Mex 104: 53-92. 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. 2001ORTEGA, M. M., GODÍNEZ-ORTEGA, J. L. & GARDUÑO-SOLÓRZANO, G. 2001. Catálogo de algas bénticas de las costas mexicanas del Golfo de México y Mar Caribe. Comisión Nacional para el Estudio de la Biodiversidad y Universidad Nacional Autónoma de México. México, D.F., México., Mateo-Cid et al., 2013MATEO-CID, L.E., MENDOZA-GONZÁLEZ, A.C. AVILA-ORTIZ, A.G. & DÍAZ-MARTÍNEZ, S. 2013. Algas marinas bentónicas del litoral de Campeche, México. Acta Bot Mex 104: 53-92.).

Acknowledgments

The authors acknowledge the Instituto Politécnico Nacional (SIP-20161052, 20164274, 20170696, 20170767), which provided financial assistance, facilities and equipment necessary for the development of this study. The first two authors thank the Instituto Politécnico Nacional and the Comisión de Operación y Fomento de Actividades Académicas del I.P.N. for the fellowships granted ACMG and LEMC thank EDI/IPN.

References

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