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Inventory of red algae (Rhodophyta) from the Sian Ka’an Biosphere Reserve, Mexican Caribbean

Inventário de algas vermelhas da Reserva da Biosfera Sian Ka’an, Caribe Mexicano

Abstract

Studies of marine and estuarine red algae (Rhodophyta) are in the early stages in the littoral of the Sian Ka’an Biosphere Reserve, Mexico. The inventory of these organisms was made based on samples obtained from ten sampling during 2009 to 2015 in 22 localities, eight of them in marine and fourteen in estuarine environments. We found 182 species and subspecific taxa of Rhodophyta. The Rhodomelaceae family was the best represented with 65 taxa, followed by Ceramiaceae 13 and Delesseriaceae 12. Of the 182 taxa, 25 are new records Sian Ka’an Biosphere Reserve with Harveylithon rupestre, Spongites fruticulosus, Acrochaetium barbadense, Dasya harveyi, Chondria pumila, Spermothamnion repens, Metapeyssonnelia milleporoides and M. tangerina being new records for the Mexican Caribbean. Of the 182 species, 119 of them are epiphytes, most of them, 54, grew exclusively on other macroalgae, 29 on mangrove roots and 8 on Thalassia leaves. The floristic list is accompanied by data on seasonality, reproduction, habitat, and environment. Species diversity was compared between the winter rains, dry and rainy seasons during the period study. The Rhodophyta of the Sian Ka’an Biosphere Reserve is tropical, and the greatest diversity was found in the marine environment with 83 taxa and during the winter rains with 132.

Keywords
Seaweed; marine; estuarine

Resumo:

Os estudos de algas vermelhas marinhas e estuarinas (Rhodophyta) estão em fase inicial no litoral da Reserva da Biosfera de Sian Ka’na, México. O inventário desses organismos foi feito com base em amostras obtidas em oito amostragens no período do 2009 a 2015 em 22 localidades, sendo oito em ambientes marinhos e quatorze em ambientes estuarinos. Neste levantamento, foram identificadas um total de 182 espécies e táxons subespecíficos de Rhodophyta. A família Rhodomelaceae foi a mais representativa com 65 táxons, seguida por Ceramiaceae com 13 e Delesseriaceae com 12. Dos 182 táxons, 25 são referidos pela primeira vez para a Reserva da Biosfera Sian Ka’an, sendo Harveylithon rupestre, Spongites fruticulosus, Acrochaetium barbadense, Dasya harveyi, Chondria pumila, Spermothamnion repens, Metapeyssonnelia milleporoides e M. tangerina também novos registros para o Caribe mexicano. Das 182 espécies, 119 são epífitas, sendo a maioria, 54, aderidas exclusivamente em outras macroalgas, 29 em raízes de mangue e 8 em folhas de Thalassia. A lista florística apresentada é acompanhada de dados sobre sazonalidade, reprodução, habitat e ambiente. A diversidade de espécies foi comparada entre as temporadas de chuvas de inverno, seca e chuvas de verão durante o período estudado. Rhodophyta da Reserva da Biosfera Sian Ka’an săo tropicais, e a diversidade mais representativa foi encontrada no ambiente marinho com 83 táxons e durante as chuvas de inverno com um total de 132 táxons.

Palavras-chave
Algas; marinhas; estuarinas

Introduction

Most of the marine benthic macroalgae are Rhodophyta and there are 7,475 species, which constitutes the highest diversity of all the large groups of macroalgae (Guiry & Guiry 2023GUIRY, M.D. & GUIRY, G.M. 2023. World-wide electronic Publication. National University of Ireland. Galway, Ireland. https://www.algaebase.org. (last access in 18/08/2023).
https://www.algaebase.org...
). Red algae develop at all latitudes and are found in greater numbers in temperate and tropical, far surpassing the remaining macroalgae groups (García-García et al. 2020GARCÍA-GARCÍA, A.M.E., CABRERA-BECERRIL, E., NÚÑEZ-RESENDIZ, M.L., DRECKMANN, K.M. & SENTÍES, A. 2020. Actualización taxonómica de las algas rojas (Rhodophyta) marinas bentónicas del Atlántico mexicano. Acta Bot. Mex. (127). e1677. DOI: 10.21829/abm127.2020.
https://doi.org/10.21829/abm127.2020...
, Guiry & Guiry 2023GUIRY, M.D. & GUIRY, G.M. 2023. World-wide electronic Publication. National University of Ireland. Galway, Ireland. https://www.algaebase.org. (last access in 18/08/2023).
https://www.algaebase.org...
). In addition to their specific richness, the Rhodophyta are primary producers and participate in ecological processes such as recruitment niches, fish and invertebrate nurseries, coralline red algae also are important components of coral reefs (Ceballos-Corona et al. 2019CEBALLOS-CORONA, J.G.A., MENDOZA-GONZÁLEZ, A.C., MATEO-CID, L.E., NÚÑEZ VARGAS, A. & SÁNCHEZ-HEREDIA, J.D. 2019. Macroalgas bentónicas marinas. In A. Cruz-Angón & K. C. Nájera-Cordero (Eds.). La Biodiversidad en Michoacán. Estudio de Estado II. Vol. 2 (p. 115−124). Ciudad de México: CONABIO.). Mexican Caribbean is one of the shoreline areas having the greatest red seaweeds diversity in Mexico (García-García et al. 2020GARCÍA-GARCÍA, A.M.E., CABRERA-BECERRIL, E., NÚÑEZ-RESENDIZ, M.L., DRECKMANN, K.M. & SENTÍES, A. 2020. Actualización taxonómica de las algas rojas (Rhodophyta) marinas bentónicas del Atlántico mexicano. Acta Bot. Mex. (127). e1677. DOI: 10.21829/abm127.2020.
https://doi.org/10.21829/abm127.2020...
); however, the area has not been well explored, suggesting that species diversity is not entirely known. The red seaweeds around the Sian Ka’an Biosphere Reserve (RBSK) had been investigated mainly during 1989–1992 and the last contribution was eight years ago. Currently, 168 species of red marine and estuarine algae are reported (Taylor 1972TAYLOR, W. R. 1972. Marine algae of the Smithsonian-Bredin expedition to Yucatán-1960. Bull. Mar. Sci. 22: 34–44., Aguilar-Rosas et al. 1989AGUILAR-ROSAS, M., AGUILAR-ROSAS, L. & HERNÁNDEZ PRIETO, J. 1989. Algas marinas bentónicas de la Bahía de la Ascensión, Quintana Roo, México. Bol. Inst. Oceanog. Ven. 28:67–75., 1992AGUILAR-ROSAS, L., AGUILAR-ROSAS, M., GÓMEZ-PEDROSO, A. & FERNÁNDEZ-PRIETO, J. 1992. Adiciones a la flora marina del Caribe Mexicano. Acta Bot. Mex. 19:77–84., 1998AGUILAR-ROSAS, M., AGUILAR-ROSAS, L. & AGUILAR-ROSAS, R. 1998. Algas marinas de la región central de Quintana Roo, México. Polibotánica. 7:15–32., Aguilar-Rosas 1990AGUILAR-ROSAS, M. 1990. Algas marinas bentónicas de la Reserva de la Biosfera de Sian Ka’an, Quintana Roo, México. In: Navarro, L.D. & Robinson, J.G. (Eds.) Diversidad Biológica de la Reserva de la Biosfera de Sian Ka’an, Quintana Roo, México, CIQRO, p. 13–34., Keeney 1999KEENEY, T.S. 1999. Coral reef macroalgae in northern Sian Ka’an Biosphere Reserve, Quintana Roo, Mexico. M.S. Thesis. Biology Program, Texas A&M University-Corpus Christi., Mendoza-González & Mateo-Cid 2007MATEO-CID, L.E. & MENDOZA-GONZÁLEZ, A.C. 2007. Flora ficológica: Diversidad, importancia económica y conservación. In: Mejía-Ortiz, L.M. (ed.). Biodiversidad acuática de la isla de Cozumel. Universidad de Quintana Roo - Plaza y Valdés. México D.F., México. 420 p., Valadez-Cruz et al. 2014VALADEZ-CRUZ, F., ROSILES-GONZÁLEZ, G. & ORTEGA-RUBIO, A. 2014. Diversidad de algas en la Reserva de la Biósfera Sian Ka’an, Quintana Roo. Investigación y Ciencia [in line] 2014, 22 (Marzo-): [Fecha de consulta: 3 de abril de 2021] Disponible en: http://www.redalyc.org/articulo.oa?id=67431160004. ISSN 1665-4412.
http://www.redalyc.org/articulo.oa?id=67...
, Mateo-Cid et al. 2014MATEO-CID, L.E., MENDOZA-GONZÁLEZ, A.C. & GABRIELSON, P.W. 2014. Neogoniolithon (Corallinales, Rhodophyta) on the Atlantic coast of Mexico, including N. siankanensis sp. nov. Phytotaxa. 190:64–93., García-García et al. 2020GARCÍA-GARCÍA, A.M.E., CABRERA-BECERRIL, E., NÚÑEZ-RESENDIZ, M.L., DRECKMANN, K.M. & SENTÍES, A. 2020. Actualización taxonómica de las algas rojas (Rhodophyta) marinas bentónicas del Atlántico mexicano. Acta Bot. Mex. (127). e1677. DOI: 10.21829/abm127.2020.
https://doi.org/10.21829/abm127.2020...
). Now, the marine life of RBSK is threatened due to the overexploitation of natural resources, urbanization, and the other anthropogenic activities (Espejel-Montes 1983ESPEJEL-MONTES, J. 1983. Biología Acuática. Descripción general de los recursos bióticos y económicos. In: Centro de Investigaciones de Quintana Roo (Ed.). Sian Ka’an: Estudios preliminares de una zona de Quintana Roo, propuesta como Reserva de la Biosfera. Centro de Investigaciones de Quintana Roo, Distrito Federal, p. 194–215., Convención RAMSAR 2003CONVENCIÓN RELATIVA A LOS HUMEDALES DE IMPORTANCIA INTERNACIONAL ESPECIALMENTE COMO HÁBITAT DE AVES ACUÁTICAS (RAMSAR). 2003. Ficha Informativa de los humedales Sian Ka’an. Ramsar.). In this context, the use of marine algae as ecological indicators is essential in monitoring the reserve. However, its application is still not possible due to the absence of a reliable and updated list (Cepeda-González et al. 2007CEPEDA-GONZÁLEZ, M.F., LASCH, T., ORTIZ, A.O., URSÚA, F.E., MEREDIZ, G., FRANQUESA, A., BERMÚDEZ, D.M., MORALES, J.A. & REZA, M. 2007. Programa de Monitoreo del Plan de Conservación del Complejo Sian Ka’an., México. The Nature Conservancy-Comisión Nacional de Áreas Naturales Protegidas-Amigos de Sian Ka’an, A.C.-United States Agency for International Development, Mérida.). Therefore, this study complements the knowledge of the three groups of seaweeds (green, brown, and red algae) that inhabit the RBSK, and the goal of this study is to update red algae list with new records and to revise the information of this group in the RBSK, with additional information as distribution, seasonality, environment, reproduction, habitat, epiphytism, and observations.

Material and Methods

Materials, methods, and description of the study area in this work are those described by Acosta-Calderón et al. (2016)ACOSTA-CALDERÓN, J.A., MATEO-CID, L.E. & MENDOZA-GONZÁLEZ, A.C. 2016. An updated list of marine green algae (Chlorophyta, Ulvophyceae) from the Biosphere Reserve of Sian Ka’an, Quintana Roo, Mexico. Checklist. 12(3):1–15. https://doi.org/10.15560/12.3.1886.
https://doi.org/10.15560/12.3.1886...
. Red algae were collected in 22 locations along the RBSK coastline (Figure 1) from March 2009 to April 2015, through ten samplings in three climatic seasons. The specimens were obtained from different substrates that Rhodophyta require for their fixation and development, such as rocks, pebbles, seagrass meadows, mainly Thalassia testudinum Banks ex König, mangrove roots, coral skeletons and mollusk remains. The plants were collected by hand with the help of spatulas and field knives at the intertidal level and at the subtidal level by free diving to a depth of four meters. The collections were made in segments of the beaches of approximately 500 m in length. Four samplings were carried out in the rainy season, two in the winter rainy season (Northern) and four in the dry season, data on the GPS coordinates of the localities, substratum, wave exposure, marine or estuarine region, and maximum depth collection of the 22 sampling sites were recorded at Table 1. Specimens of nongeniculate coralline algae were borrowed from ENCB (Departamento de Botánica, Escuela Nacional de Ciencias Biológicas del Instituto Politécnico Nacional, CDMX, Mexico). Additional specimens of nongeniculate coralline algae were collected by reef-walking or snorkeling. Samples were preserved in 5% formalin/seawater for anatomical observations; duplicate samples of some specimens were preserved in silica gel for molecular analyses. Formalin preserved specimens were decalcified with 0.6M HNO3 and dehydrated with ethyl alcohol at different concentrations: 10%, 20%, 30%, 40%, 50%, 60%, 70%, 80%, 90% and absolute ethyl alcohol (Mateo-Cid et al. 2014MATEO-CID, L.E., MENDOZA-GONZÁLEZ, A.C. & GABRIELSON, P.W. 2014. Neogoniolithon (Corallinales, Rhodophyta) on the Atlantic coast of Mexico, including N. siankanensis sp. nov. Phytotaxa. 190:64–93.). Small fragments were embedded in paraffin and sectioned 9–12 μm thick with a manual microtome, fixed on slides with Riuter’s adhesive (Martoja & Martoja-Pierson 1970MARTOJA, R. & MARTOJA-PIERSON, M. 1970. Técnicas de Histología Animal. Barcelona: Toray-Masson. 370 p.), and stained with aniline blue and hematoxilin eosine for anatomical observations and measurements. Procedures for morphological observations followed Kato et al. (2006); specimens for molecular analyses were deposited in NCU with duplicates in ENCB. Silica gel-dried samples for DNA extraction were examined under high magnification with a dissecting microscope to check for red algal epiphytes. Clean fragments about 3 mm3 total volume were placed in heavy paper packets and crushed and ground to a fine powder before being extracted following the protocol in Hughey et al. (2001)HUGHEY, J.R., SILVA, P.C. & HOMMERSAND, M.H. 2001. Solving taxonomic and nomenclatural problems in Pacific Gigartinaceae (Rhodophyta) using DNA from type material. J Phycol. 37: 1091–1109. https://dx.doi.org/10.1046/j.1529-8817.2001.01048.x.
https://doi.org/10.1046/j.1529-8817.2001...
and the recommendations in Hughey & Gabrielson (2012)HUGHEY, J. & GABRIELSON, P.W. 2012. Comment on “Acquiring DNA sequence data from dried archival red algae (Florideophyceae) for the purpose of applying available names to contemporary genetic species: a critical assessment” Botany. 90:1191–1194. https://dx.doi.org/10.1139/b2012-102.
https://doi.org/10.1139/b2012-102...
. For DNA sequencing of collected specimens, markers chosen for PCR included the chloroplast-encoded genes rbcL, psbA as well as COI, and LSU (Richards et al. 2021RICHARDS, J.L., SCHMIDT, W.E., FREDERICQ, S., SAUVAGE, T., PEÑA, V., LE GALL, L., MATEO-CID, L.E., MENDOZA-GONZÁLEZ, A.C., HUGHEY, J.R. & GABRIELSON, P.W. 2021. DNA sequencing of type material and newly collected specimens reveals two homotypic synonyms for Harveylithon munitum (Metagoniolithoideae, Corallinales, Rhodophyta) and three new species. J Phycol. 57:1234–1253. https://doi.org/10.1111/jpy.13161.
https://doi.org/10.1111/jpy.13161...
). DNA was extracted from globally collected specimens at the University of North Carolina at Chapel Hill following the protocol established by Hughey et al. (2001)HUGHEY, J.R., SILVA, P.C. & HOMMERSAND, M.H. 2001. Solving taxonomic and nomenclatural problems in Pacific Gigartinaceae (Rhodophyta) using DNA from type material. J Phycol. 37: 1091–1109. https://dx.doi.org/10.1046/j.1529-8817.2001.01048.x.
https://doi.org/10.1046/j.1529-8817.2001...
and modified by Gabrielson et al. (2011)GABRIELSON, P.W., MILLER, K.A. & MARTONE, P.T. 2011. Morphometric and molecular analyses confirm two distinct species of Calliarthron (Corallinales, Rhodophyta), a genus endemic to the northeast Pacific. Phycologia. 50:298–316. for coralline algae. Amplification of psbA, rbcL, UPA, COI, and LSU followed the protocols and primers described in Richards et al. (2014RICHARDS, J. L., GABRIELSON, P. W. & FREDERICQ, S. 2014. New insights into the genus Lithophyllum (Lithophylloideae; Corallinaceae, Corallinales) from offshore the NW Gulf of Mexico. Phytotaxa. 190:162–75., 2016RICHARDS, J.L., VIEIRA-PINTO, T., SCHMIDT, W.E., SAUVAGE, T., GABRIELSON, P.W., OLIVEIRA, M.C. & FREDERICQ, S. 2016. Molecular and morphological diversity of Lithothamnion spp. (Hapalidiales, Rhodophyta) from deepwater rhodolith beds in the Northwestern Gulf of Mexico. Phytotaxa. 278:81–114.). Voucher specimens are deposited in the herbarium of the Escuela Nacional de Ciencias Biológicas located in Mexico City, Mexico (ENCB), herbarium acronym follows Index Herbariorum (Thiers 2023THIERS, B. 2023. Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. Available at: http://sweetgum.nybg.org/science/ih/ (last accessed 15 August 2023).
http://sweetgum.nybg.org/science/ih/...
). Also, information on species previously collected by other researchers was obtained of the herbarium ENCB; the determinations of some specimens were corrected and finally a bibliographic review of the studies carried out in the SKBR from 1989 to 2015, to obtain the records of Rhodophyta previously cited for the coast of the state and thereby compare it with the data obtained in the present study. To describe the geographical distribution of marine algae, 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 number of Phaeophyceae species), useful for knowing the geographical areas where algae are distributed and thus classifying the flora of a given region as a function of the latitudinal gradient. Thus, a value of the ratio R/P > 4 is found in tropical regions, while R/P < 2 corresponds to the phycoflora of temperate-cold regions. Cheney (1977)CHENEY, D.P. 1977. A new improved ratio for comparing seaweed floras. J. Phycol. 13(suppl.):1–13. included the Chlorophyta (C) in an index like the one previously exposed (R + C)/P and showed that values of the ratio (R + C)/P ≥ 6 are obtained in tropical floras, while those from temperate-cold seas have indices <3, intermediate values suggest a mixed flora. The floristic list is accompanied by data on distribution, seasonality, environment, reproduction, habitat, observations, and herbarium number, new records for the RBSK and for Mexican Caribbean are indicated in Table 2. Species names are according to Wynne (2022)WYNNE, M.J. 2022. Checklist of benthic marine algae of the tropical and subtropical Western Atlantic: fifth revision. Nova Hedwigia Beiheft. 153:1–180. and Guiry & Guiry (2023)GUIRY, M.D. & GUIRY, G.M. 2023. World-wide electronic Publication. National University of Ireland. Galway, Ireland. https://www.algaebase.org. (last access in 18/08/2023).
https://www.algaebase.org...
.

Figure 1.
Study area.
Table 1.
Substrate characteristic, wave exposure, region, and maximum depth collection of the 22 sampling sites in the RBSK, Quintana Roo, Mexico. BA: Ascension, BE: Espiritu Santo bays.
Table 2.
Rhodophyta of the Sian Ka’an Biosphere Reserve, Quintana Roo (2009–2015). (The abbreviations are explained at the end of the table).

Results

1. Floristics

During the study period (March 2009 to April 2015), 182 Rhodophyta taxa distributed in 4 classes, 15 Orders, 30 Families and 83 genera were determined (Table 2). The best represented Order was Ceramiales with 104 taxa (57.1%) followed by Corallinales with 29 (15.9%). The best represented families were Rhodomelaceae with 65 taxa (35.7%), followed by Ceramiaceae 13 (7.1%), Delesseriaceae with 12 (6.6%) and Spongitidaceae 10 (5.4%). Species of Bangiaceae, Liagoraceae, Galaxauraceae, Gelidiaceae, Cystocloniaceae, Peyssonneliaceae and Gracilariaceae represented by 1 or 5 species were also located (Table 2). The most representative genera in terms of the number of species were Chondria with 12, Neogoniolithon and Laurencia with 9 each, Ceramium, Dasya and Polysiphonia with 8 each. Bangia, Asparagopsis, Lithothamnion, Melobesia, Wrightiella, Vertebrata, Gelidium and Gelidiella, among others, are unispecific. The Rhodophyta determined in this work have been recorded in the tropical and temperate rocky areas of the world, including the coast of the Gulf of Mexico and the Mexican Caribbean (Wynne 2022WYNNE, M.J. 2022. Checklist of benthic marine algae of the tropical and subtropical Western Atlantic: fifth revision. Nova Hedwigia Beiheft. 153:1–180., García-García et al. 2020GARCÍA-GARCÍA, A.M.E., CABRERA-BECERRIL, E., NÚÑEZ-RESENDIZ, M.L., DRECKMANN, K.M. & SENTÍES, A. 2020. Actualización taxonómica de las algas rojas (Rhodophyta) marinas bentónicas del Atlántico mexicano. Acta Bot. Mex. (127). e1677. DOI: 10.21829/abm127.2020.
https://doi.org/10.21829/abm127.2020...
). Considering previous studies of the studies of Acosta-Calderón et al. (2016)ACOSTA-CALDERÓN, J.A., MATEO-CID, L.E. & MENDOZA-GONZÁLEZ, A.C. 2016. An updated list of marine green algae (Chlorophyta, Ulvophyceae) from the Biosphere Reserve of Sian Ka’an, Quintana Roo, Mexico. Checklist. 12(3):1–15. https://doi.org/10.15560/12.3.1886.
https://doi.org/10.15560/12.3.1886...
and Mateo-Cid et al. (2019)MATEO-CID, L.E., MENDOZA-GONZÁLEZ, A.C. & HERNÁNDEZ CASAS, C.M. 2019. Diversity of brown algae (Ochrophyta, Phaeophyceae) of Sian Ka’an Reserve Biosphere, Mexican Caribbean. Pak. J. Bot. 51(1), DOI: 10.30848/PJB2019-1(40).
https://doi.org/10.30848/PJB2019-1(40)...
who listed the Chlorophyta and Phaeophyceae, respectively, from the RBSK, the Feldmann and Cheney indexes were calculated and compared with other localities and states of the Yucatan Peninsula (Table 3). Both the Feldmann and Cheney indices indicate that the RBSK phycoflora is of tropical affinity.

Table 3.
Species not located in the study period (Reported by Valadez-Cruz et al., 2014VALADEZ-CRUZ, F., ROSILES-GONZÁLEZ, G. & ORTEGA-RUBIO, A. 2014. Diversidad de algas en la Reserva de la Biósfera Sian Ka’an, Quintana Roo. Investigación y Ciencia [in line] 2014, 22 (Marzo-): [Fecha de consulta: 3 de abril de 2021] Disponible en: http://www.redalyc.org/articulo.oa?id=67431160004. ISSN 1665-4412.
http://www.redalyc.org/articulo.oa?id=67...
, García-García et al. 2020GARCÍA-GARCÍA, A.M.E., CABRERA-BECERRIL, E., NÚÑEZ-RESENDIZ, M.L., DRECKMANN, K.M. & SENTÍES, A. 2020. Actualización taxonómica de las algas rojas (Rhodophyta) marinas bentónicas del Atlántico mexicano. Acta Bot. Mex. (127). e1677. DOI: 10.21829/abm127.2020.
https://doi.org/10.21829/abm127.2020...
).

2. New records

The integration of the floristic list allowed us to recognize 25 new infrageneric records for the RBSK coastline, including Harveylithon rupestre, Spongites fruticulosus, Acrochaetium barbadense, Dasya harveyi, Chondria pumila, Spermothamnion repens, Metapeyssonnelia milleporoides and M. tangerina, representing new records for the Mexican Caribbean. Of the 168 previous infrageneric records, 116 taxa were found in this study and 51 were not found in the collected samples. Due to the above, the number of species recorded for the coast of the Sian Ka’an Biosphere Reserve increased to 233 infrageneric taxa of benthic marine and estuarine red algae, which represents an increase of 28% of the total Rhodophyta in the study area. Most of the new records for RBSK belong to genera of coralline algae and the Rhodomelaceae family such as Chondria and Laurencia.

3. Temporal variation

Figure 2 represents the number of taxa identified by climatic season, in general we can observe high richness in the three seasons, being in winter rains (northern) when the highest specific richness was located with 132, followed by rainy, 122 and finally dry with 107 taxa. Figure 3 shows the number of taxa per locality, it is observed that the locality corresponding to Punta Pelícanos presented the greatest richness (96 taxa), followed by Punta Xoquem (49) and Hualapich (45). The three localities have in common the fact of being found in a marine environment and be rocky beaches. The localities with the lowest specific richness are Golfito (11), Punta Allen and Golfito (10) and Punta Mosquitero (7), the first three are in an estuarine environment and only Punta Mosquitero is in a marine environment.

Figure 2.
Number of taxa by climatic season.
Figure 3.
Number of taxa per locality.

The number of taxa found in the different environments is represented in Figure 4, where it is observed that the highest species richness was found in the marine environment with 83 taxa, while in the estuarine environment 34 and 65 were found inhabiting in both marine and estuarine environments (Table 2).

Figure 4.
Number of taxa by environment.

4. Reproduction

The reproductive phase that was found most frequently in this study was the tetrasporic, which exceeded both the algae found with male or female gametic phase. These data allow us to consider that this generation has a longer survival with respect to the gametophytic generation, and other reproductive mechanisms such as vegetative propagation or apomeiosis. From the 182 taxa located in this study, 92.3% (168) were found in the fertile stage and only 7.6% (14) were found in the vegetative state, the sporophytic phase was found in 153 taxa, the gametophytic phase exclusively in 12 and finally 44 taxa and they were found both in the sporophytic phase (sporophyte and carposporophyte) and in the gametophytic phase (Table 2).

5. Epiphytism

Altogether 119 epiphytic taxa were identified (Table 2), by host we have that, from them, 54 grew exclusively on other Rhodophyta, 29 lived on the roots or bark of mangrove (Rhizophora mangle Linnaeus), 8 in Thalassia testudinum Banks ex König, 12 both in mangrove as in other Rhodophyta, 7 in other Rhodophyta and Thalassia, only 3 were inhabitants of both T. testudinum and mangrove roots and finally 6 taxa were located in all hosts (Figure 5). The highest number of epiphytes was obtained in the dry season with 92, observing the highest number of species of the families Rhodomelaceae, Wrangeliaceae and Ceramiaceae.

Figure 5.
Number of epiphytes by host (abbreviations = Mg = Rhizophora mangle, Th = Thalassia testudinum, Sw = Other macroalgae).

Discussion

1. Floristics

The total number of taxa found in this study is greater than that recorded on the coast of the island of Cozumel Mateo-Cid & Mendoza-González (1991)MATEO-CID, L.E. & MENDOZA-GONZÁLEZ, A.C. 1991. Algas marinas bénticas de la Isla Cozumel, Quintana Roo, México. Acta Bot. Mex. 16:57–87. DOI: https://doi. org/10.21829/abm16.1991.626
https://doi.org/10.21829/abm16.1991.626...
cited 168 Rhodophyta taxa; Mateo-Cid & Mendoza-González (1992)MENDOZA-GONZÁLEZ, A.C. & MATEO-CID, L.E. 1992. Algas marinas bentónicas de Isla Mujeres, Quintana Roo, México. Acta Bot. Mex. 19:37–61. DOI: https://doi. org/10.21829/abm19.1992.646.
https://doi.org/10.21829/abm19.1992.646...
recorded 122 red algae off the coast of Isla Mujeres; 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. recorded 109 Rhodophyta in Puerto Morelos. On the other hand, Cetz-Navarro et al. (2008)CETZ-NAVARRO, N.P., ESPINOZA-AVALOS, J., SENTÍES, A. & QUAN YOUNG, L.I. 2008. New records of macroalgae for the Mexican Atlantic and floristic richness of the Mexican Caribbean. Hidrobiológica. 18(1):11–19. listed 53 Rhodophyta taxa for Quintana Roo in works after the catalog by Ortega et al. (2001)ORTEGA, M.M., GODÍNEZ, J.L. & GARDUÑO-SOLÓRZANO, G. 2001. Catálogo de algas bénticas de las costas mexicanas del Golfo de México y Mar Caribe. Instituto de Biología, Universidad Nacional Autónoma de México (UNAM) y Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO). México, D.F. 594 p.. In the case of Valadez-Cruz et al. (2014)VALADEZ-CRUZ, F., ROSILES-GONZÁLEZ, G. & ORTEGA-RUBIO, A. 2014. Diversidad de algas en la Reserva de la Biósfera Sian Ka’an, Quintana Roo. Investigación y Ciencia [in line] 2014, 22 (Marzo-): [Fecha de consulta: 3 de abril de 2021] Disponible en: http://www.redalyc.org/articulo.oa?id=67431160004. ISSN 1665-4412.
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these authors documented 172 Rhodophyta taxa for the Sian Ka’an Biosphere Reserve, which shows that the RBSK has a great specific richness of red algae from the Quintana Roo coast, with numerous taxa characteristic of the region. In addition, the results obtained suggest that the RBSK is an area with high floristic diversity, if one considers that 50.4% of the Rhodophyta known for the coast of Quintana Roo can be found on its coastline, which is 451 species and 13 infraspecific categories of red algae (García-García et al. 2020GARCÍA-GARCÍA, A.M.E., CABRERA-BECERRIL, E., NÚÑEZ-RESENDIZ, M.L., DRECKMANN, K.M. & SENTÍES, A. 2020. Actualización taxonómica de las algas rojas (Rhodophyta) marinas bentónicas del Atlántico mexicano. Acta Bot. Mex. (127). e1677. DOI: 10.21829/abm127.2020.
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).

The best represented family in our study was Rhodomelaceae with 65 taxa, a figure greater than that found by Mateo-Cid & Mendoza-González (1991)MATEO-CID, L.E. & MENDOZA-GONZÁLEZ, A.C. 1991. Algas marinas bénticas de la Isla Cozumel, Quintana Roo, México. Acta Bot. Mex. 16:57–87. DOI: https://doi. org/10.21829/abm16.1991.626
https://doi.org/10.21829/abm16.1991.626...
where the authors recorded 38 Rhodomelaceae taxa for Cozumel 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. cite 34 for Puerto Morelos and Senties & Dreckmann (2014)SENTIES, A. & DRECKMANN, K.M. 2014. Diversidad de las macroalgas marinas de la familia Rhodomelaceae (Rhodophyta) en México. Rev. Mex. Biodiv. 85:62–68. recorded 26 species of the Rhodomelaceae family for the coast of Campeche. On the other hand, Senties & Dreckmann (1990)SENTÍES, A. & DRECKMANN, K.M. 1990. La familia Rhodomelaceae (Ceramiales, Rhodophyta) en la costa del estado de Michoacán México. Bol. Soc. Bot. Mex. 50:89–120. indicate that the Rhodomelaceae family (order Ceramiales) is the most numerous not only within the Order, but also within the Rhodophyta division. The species of this order have a greater affinity for tropical, subtropical, and temperate zones, occupying mostly rocky substrates and some epiphytes in intertidal and subtidal environments, characteristics that our study locations present. The specific richness and the presence of the species of the order Ceramiales in all the localities of the RBSK can be explained in several ways; one of them is that red algal order Ceramiales contains the 37.6% of all floridean red algal species (Guiry & Guiry 2023GUIRY, M.D. & GUIRY, G.M. 2023. World-wide electronic Publication. National University of Ireland. Galway, Ireland. https://www.algaebase.org. (last access in 18/08/2023).
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). It is a highly diverse group in terms of number of species, with over 330 genera and over 2690 species. The order is represented in all marine and brackish habitats worldwide and is comprised of five families: Callithamniaceae, Ceramiaceae, Delesseriaceae, Rhodomelaceae and Wrangeliaceae (Guiry & Guiry 2023GUIRY, M.D. & GUIRY, G.M. 2023. World-wide electronic Publication. National University of Ireland. Galway, Ireland. https://www.algaebase.org. (last access in 18/08/2023).
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). In addition to their high diversity, the Ceramiales have a great adaptability to develop in different environments. For example, the Rhodomelaceae species occupy various marine habitats: they can grow as free-living plants on stones, rocks, shells, and different artificial substrata, or colonize other algae either as obligate epiphytes or as parasites. Also, there are cosmopolitan species growing within a broad range of temperature (0–28 °C), salinity (6.0–32.5‰), and vertical distribution. In different locations it may occur in the low-intertidal zone, in rock pools, in shallow or deep (15–17 m) subtidal water along open, wave-exposed coasts and in sheltered habitats (Tarakhovskaya et al. 2022TARAKHOVSKAYA, E., ZUY, E., YANSHIN, N., & ISLAMOVA, R. 2022. Concise review of the genus Vertebrata SF Gray (Rhodophyta: Ceramiales). J Appl. Phycol. 34(5): 2225–2242.). On the other hand, many studies show that the species of the order Ceramiales are successful, due to their asexual reproduction and the vegetative multiplication mechanisms as fragmentation, multicellular propagules, and monopodial stoloniferous growth (Kilar & McLachlan 1986KILAR, J.A., & MCLACHLAN, J. 1986. Ecological studies of the alga, Acanthophora spicifera (Vahl) Boerg. (Ceramiales: Rhodophyta): vegetative fragmentation. J. Exp. Mar. Biol. Ecol. 104(1–3):1–21., Kapraun 1977KAPRAUN, D.F. 1977. Asexual propagules in the life history of Polysiphonia ferulacea (Rhodophyta, Ceramiales). Phycologia. 16(4):417–426., Haroun & Gil-Rodriguez 1995HAROUN R.J. & GIL-RODRIGUEZ, M.C. 1995. Reproductive strategies of Laurencia perforata (Bory) Montagne (Ceramiales, Rhodomelaceae) in the Canary Islands. Nova Hedwigia. 61:269–274., Husa & Sjøtun 2006HUSA, V., & SJØTUN, K. 2006. Vegetative reproduction in “Heterosiphonia japonica” (Dasyaceae, Ceramiales, Rhodophyta), an introduced red alga on European coasts. Bot. Mar. 49:191–199. https://doi.org/10.1515/BOT.2006.024.
https://doi.org/10.1515/BOT.2006.024...
, Cecere et al. 2007CECERE, E., PETROCELLI, A., & PERRONE, C. 2007. How the unattached form of Acanthophora nayadiformis (Rhodophyta: Ceramiales) produces storage and perennating organs. J Mar. Biolog. Assoc. UK. 87(2):389–392.).

Of the 182 taxa determined in this study for the RBSK coastline, 25 represent new records for the study area (NRSK) and of these, 8 are new records for the Mexican Caribbean (Table 2); on the other hand, 51 previously recorded species were not located (Table 3), perhaps due to changes in the environments where these algae inhabit, where there is currently a greater human influence that has modified the architecture of the landscape, as well as natural events such as hurricanes and Tropical storms. Entirety, previous records, and those obtained in this study constitute a total of 233 registered species for the RBSK, however, it is important to highlight that the Espiritu Santo Bay has not been sufficiently studied, so to know the phycofloristic composition throughout the reserve, more studies are required in this bay.

There are also doubtful records of some species, to name a few, 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. in their work on the morphological and molecular characterization of the genus Centroceras, found that samples identified under the concept of “Centroceras clavulatum” represented 9 morphological groups that corresponded to different clades in their phylogenetic analysis and determined that the distribution of C. clavulatum is restricted to northern Chile, Peru, southern California, southern Australia and New Zealand, which makes its presence in the Mexican Caribbean region unlikely. Díaz-Tapia et al. (2017)DÍAZ-TAPIA, P., MCIVOR, L., FRESHWATER, D.W., VERBRUGGEN, H., WYNNE, M.J. & MAGGS, C.A. 2017. The genera Melanothamnus Bornet et Falkenberg and Vertebrata S.F. Gray constitute well-defined clades of the red algal tribe Polysiphonieae (Rhodomelaceae, Ceramiales). Eur. J. Phycol. 52, 1−20. https://doi.org/10.1080/09670262.2016.1256436
https://doi.org/10.1080/09670262.2016.12...
sought to clarify the relationships in the Neosiphonia/Polysiphonia complex using a combination of molecular and morphological analyses, based on their results they transferred 46 species of Neosiphonia to Melanothamnus, including Melanothamnus hawaiiensis (type locality: Waikiki, Oahu, Hawaiian Islands) also indicating, the distribution of the genus Melanothamnus is predominantly in the Indo-Pacific, so it is necessary to reevaluate the species of the genus Melanothamnus that have been cited in the Mexican Caribbean.

Particularly for the genus Jania, it is widely known about its complicated scenario to establish limits between species due to the substantial morphological variation that it exhibits, consequently, the correct application of names for many species of Jania is surrounded by uncertainty and, therefore, lacks knowledge of a stable nomenclatural foundation, and descriptions are often brief and inadequate as well (Harvey et al. 2020HARVEY, A.S., WOELKERLING, W.J. & REVIERS, B. DE. 2020. A taxonomic analysis of Jania (Corallinaceae, Rhodophyta) in south-eastern Australia. Aust. Syst. Bot. 33:221–277.). Harvey et al. (2020)HARVEY, A.S., WOELKERLING, W.J. & REVIERS, B. DE. 2020. A taxonomic analysis of Jania (Corallinaceae, Rhodophyta) in south-eastern Australia. Aust. Syst. Bot. 33:221–277. in a study of the genus Jania in Australia evaluated 79 diagnostic characters to delimit the species of this genus, finding that many of these characters’ overlap each other or are inadequately explained, some characters or character states were not found in species from south-eastern Australia or its nomenclatural types and therefore could not be assessed. Others were present in all specimens and thus were of no value in delineating species found in south-eastern Australia and which records of some species from south-eastern Australia involve misidentified specimens. In their study, Harvey et al. (2020)HARVEY, A.S., WOELKERLING, W.J. & REVIERS, B. DE. 2020. A taxonomic analysis of Jania (Corallinaceae, Rhodophyta) in south-eastern Australia. Aust. Syst. Bot. 33:221–277. transferred J. adhaerens as a synonym of Jania pedunculata var. adhaerens, indicating that, in the published literature, the concept of the morphoanatomy of J. adhaerens varies considerably from publication to publication. In addition, there is no consensus in the literature regarding what defines J. adhaerens as a species from a morphoanatomical point of view, so it is necessary to review the type of material and molecular sequence data may also be useful. Finally, the authors excluded J. rubens from south-eastern Australia because the records are based on misidentifications. The type locality of J. rubens is ‘Insulae Stoechades’ [Îles d’ Hyères, Francia, Mediterráneo], in the prologue Linnaeus (1758LINNAEUS, C. 1758. Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima, reformata. Editio decima revisa. Vol. 1 p. [i–iv], [1]-823. Holmiae [Stockholm]: impensis direct. Laurentii Salvii., p. 806) indicated ‘Habitat en Oceano Europæo’ and it is not known whether this includes the Mediterranean (Guiry & Guiry 2023GUIRY, M.D. & GUIRY, G.M. 2023. World-wide electronic Publication. National University of Ireland. Galway, Ireland. https://www.algaebase.org. (last access in 18/08/2023).
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). Regarding J. tenella, the type locality is the Gulf of Naples (Italy), and the distribution of this species is mainly in the Pacific islands, Japan, and Taiwan (Guiry & Guiry 2023GUIRY, M.D. & GUIRY, G.M. 2023. World-wide electronic Publication. National University of Ireland. Galway, Ireland. https://www.algaebase.org. (last access in 18/08/2023).
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). It is evident that the Jania species cited in the Mexican Caribbean require morphological and molecular studies to find the true taxonomic and phylogenetic affinities of these species, as well as to delimit their distribution in the study area.

The use of morphoanatomical characters in the determination of non-geniculate coralline algae collected in the RBSK has been problematic; this fact is consistent with what was reported by Kato et al. (2013)KATO, A., BABA, M. & SUDA, S. 2013. Taxonomic circumscription of heterogeneous species Neogoniolithon brassica-florida (Corallinales, Rhodophyta) in Japan. Phycol. Res. 61:15–26. https://dx.doi.org/10.1111/j.1440-1835.2012.00665.x
https://doi.org/10.1111/j.1440-1835.2012...
, Mateo-Cid et al. (2014)MATEO-CID, L.E., MENDOZA-GONZÁLEZ, A.C. & GABRIELSON, P.W. 2014. Neogoniolithon (Corallinales, Rhodophyta) on the Atlantic coast of Mexico, including N. siankanensis sp. nov. Phytotaxa. 190:64–93. and Richards et al. (2021)RICHARDS, J.L., SCHMIDT, W.E., FREDERICQ, S., SAUVAGE, T., PEÑA, V., LE GALL, L., MATEO-CID, L.E., MENDOZA-GONZÁLEZ, A.C., HUGHEY, J.R. & GABRIELSON, P.W. 2021. DNA sequencing of type material and newly collected specimens reveals two homotypic synonyms for Harveylithon munitum (Metagoniolithoideae, Corallinales, Rhodophyta) and three new species. J Phycol. 57:1234–1253. https://doi.org/10.1111/jpy.13161.
https://doi.org/10.1111/jpy.13161...
, due to the above and based on sequencing only 20 specimens from the rather narrow study area, we have recovered 9 species of Neogoniolithon, and 2 Harveylithon and Porolithon each, in the case of Spongites and Lithothamnion specimens lack many morphoanatomical characters needed to adequately describe them, particularly those characters associated with reproduction. We have not sequenced any specimens that morphoanatomical we call S. fruticulosus and L. sejunctum. We recognize that acceptance of each of these names for our local species will depend upon sequencing some specimens.

2. Biogeography

The results of the present study were examined with the Feldmann and Cheney indices and were contrasted with what was found by Mateo-Cid & Mendoza-González (2007)MATEO-CID, L.E. & MENDOZA-GONZÁLEZ, A.C. 2007. Flora ficológica: Diversidad, importancia económica y conservación. In: Mejía-Ortiz, L.M. (ed.). Biodiversidad acuática de la isla de Cozumel. Universidad de Quintana Roo - Plaza y Valdés. México D.F., México. 420 p. for Isla Cozumel; Mendoza-González et al. (2007)MENDOZA-GONZÁLEZ, A.C. & MATEO-CID, L.E. 2007. Cinco nuevos registros de algas rojas (Rhodophyta) para el Caribe mexicano. Polibotánica. 23:101–119. from Isla Mujeres, 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 and Huerta-Múzquiz et al. (1987)HUERTA-MÚZQUIZ, L., MENDOZA-GONZÁLEZ, A. C. & MATEO-CID, L.E. 1987. Avance de un estudio de las algas marinas de la península de Yucatán. Phytologia. 62(1):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-MORGUEL, C. & CASANOVA-CETZ, R.A. 2007. Análisis de la biodiversidad de algas marinas situadas entre Uaymitún y Chuburná, Yucatán. Ingeniería. 11(1):43–51. for the Yucatan coast. Table 4 shows the data obtained from the Feldmann and Cheney indices calculated in the four regions mentioned; the phycoflora of the study area is similar to that obtained for the Isla Cozumel and Isla Mujeres, completely Caribbean localities. The indices used allow us to establish that the marine and estuarine algae of the Sian Ka’an Biosphere Reserve have a predominant tropical distribution and that, accordingly, the presence of Jania cubensis, Amphiroa fragilissima, A. tribulus, Neogoniolithon spectabile, Titanophycus validus, Ceramium nitens, Dasya caraibica, Bostrychia binderi, Chondria littoralis, Wrangelia penicillata, Gracilaria blodgettii and G. crassissima, were recorded among others.

Table 4.
Feldmann and Cheney indices for some marine environments of the coast of the Gulf of Mexico and the Mexican Caribbean.

3. Temporal variation

In the present work, the highest species richness was found in the northern (winter rains), followed by summer rains, and the lowest species richness was found in the dry season. This can be justified with what is reported by Pech-Poll et al. (2010)PECH-POLL, D., MASCARÓ MIQUELAJÁUREGUI, M., SIMÖES, N. & ENRÍQUEZ ORTIZ, C. 2010. Ambientes marinos. In Durán R. y M. Méndez (Eds). Biodiversidad y Desarrollo Humano en Yucatán. CICY, PPD-FMAM, CONABIO, SEDUMA. 496 p. who relate the physicochemical parameters with the abundance and diversity of species, in addition to the amount of nutrients available in the habitat, in the case of the summer or winter rainy season, the supply of nutrients is greater due to runoff along the coast, this would also justify the fact that a high species richness is present in the northern rainy climatic season, not varying in great number with the rainy season. On the other hand, the dry climatic season provides a more adverse habitat due to the low rainfall that exists in the season, as well as the high temperature that occurs, since it can reach more than 30 °C, which increases the evaporation of seawater and therefore salinity. Mateo-Cid & Mendoza-González (1991)MATEO-CID, L.E. & MENDOZA-GONZÁLEZ, A.C. 1991. Algas marinas bénticas de la Isla Cozumel, Quintana Roo, México. Acta Bot. Mex. 16:57–87. DOI: https://doi. org/10.21829/abm16.1991.626
https://doi.org/10.21829/abm16.1991.626...
mention that seasonality in the Mexican Caribbean is related to large temperature fluctuations throughout the year.

The changes in each community at each time of the year are largely regulated by the biological rhythms of the organisms that constitute it, which in turn are related to environmental fluctuations (Núñez-López 1996), which modify the physicochemical characteristics of seawater associated with the seasonality of the environment. The spatial and temporal variability is affected by factors such as the complexity of the substrate, as well as temperature and salinity, since at high atmospheric temperature water evaporation is greater, generating hot water and higher salinity, on the contrary, when there is a high rate of rainfall, a considerable discharge of fresh water is caused along the coast (Pech- Poll et al. 2010).

In this context, Punta Pelicanos, Hualapich, Punta Xoquem and Pulticub provide adequate conditions for the high specific richness of red algae that are present, this is because in the intertidal zone there are platforms and rocky plains with gentle waves, in addition these beaches are in a conserved region for being within the reserve. In the same way, the localities where there was a low specific richness correspond to Cayo Lagartijas, Cayo Xobón, Punta Allen, Isla Techal and Golfito, localities that are located within the bays, purely estuarine areas, in which there are no adequate conditions for the establishment and development of the Rhodophyta, especially the type of substrate that is mostly sandy and the presence of seagrass beds and mangroves. It is important to highlight that a high percentage of the Rhodophyta species of the Mexican Caribbean have been collected in rocky substrate, Santelices (1977)SANTELICES, B. 1977. Ecología de las algas marinas bentónicas. Universidad Católica de Chile. Santiago. 384 p., Mateo-Cid & Mendoza-González (1991)MATEO-CID, L.E. & MENDOZA-GONZÁLEZ, A.C. 1991. Algas marinas bénticas de la Isla Cozumel, Quintana Roo, México. Acta Bot. Mex. 16:57–87. DOI: https://doi. org/10.21829/abm16.1991.626
https://doi.org/10.21829/abm16.1991.626...
, Mendoza-González & Mateo-Cid (1992)MENDOZA-GONZÁLEZ, A.C. & MATEO-CID, L.E. 1992. Algas marinas bentónicas de Isla Mujeres, Quintana Roo, México. Acta Bot. Mex. 19:37–61. DOI: https://doi. org/10.21829/abm19.1992.646.
https://doi.org/10.21829/abm19.1992.646...
and Ortega et al. (2001)ORTEGA, M.M., GODÍNEZ, J.L. & GARDUÑO-SOLÓRZANO, G. 2001. Catálogo de algas bénticas de las costas mexicanas del Golfo de México y Mar Caribe. Instituto de Biología, Universidad Nacional Autónoma de México (UNAM) y Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO). México, D.F. 594 p. indicate that this substrate exposed to waves is the place where a great diversity of marine algae is located.

4. Reproduction

The reproductive stage best represented in this study was the sporic stage, which coincides with the results obtained by Mateo-Cid & Mendoza-González (1991)MATEO-CID, L.E. & MENDOZA-GONZÁLEZ, A.C. 1991. Algas marinas bénticas de la Isla Cozumel, Quintana Roo, México. Acta Bot. Mex. 16:57–87. DOI: https://doi. org/10.21829/abm16.1991.626
https://doi.org/10.21829/abm16.1991.626...
, Mendoza-González & Mateo-Cid (1992)MENDOZA-GONZÁLEZ, A.C. & MATEO-CID, L.E. 1992. Algas marinas bentónicas de Isla Mujeres, Quintana Roo, México. Acta Bot. Mex. 19:37–61. DOI: https://doi. org/10.21829/abm19.1992.646.
https://doi.org/10.21829/abm19.1992.646...
, Mateo-Cid et al. (2013)MATEO-CID, L.E., MENDOZA GONZÁLEZ, A.C., ÁVILA ORTIZ, A.G. & DÍAZ MARTÍNEZ, S. 2013. Algas marinas bentónicas del litoral de Campeche, México. Acta Bot. Mex. 104:53–92., and Lucio & Nunes (2002)LUCIO, A.M. & NUNES J.M.C. 2002. Aportación al conocimiento fenológico de las rodofíceas marinas de la playa del Guarajuba (Camacari, Bahía) Brasil. Bot. Complut. 26:17–34., the latter authors mention that the dominance of a reproductive phase may be influenced by temporary changes in local environmental factors. On the other hand, Ardito & Gómez (2005)ARDITO, S. & GÓMEZ, S. 2005. Patrón fenológico de una población de Gelidium serrulatum J. Agardh (Rhodophyta, Gelidiales) en la localidad de Taguao, Estado Vargas, Venezuela. Acta Bot. Ven. 28(1):101–111. consider that the sporophytic generation has a longer survival than the gametophytic generation, in addition to other reproductive mechanisms such as vegetative propagation or apomeiosis.

The sexual stages were poorly represented in this study, according to Santelices (1977)SANTELICES, B. 1977. Ecología de las algas marinas bentónicas. Universidad Católica de Chile. Santiago. 384 p. asexual reproduction has the advantage of requiring less energy expenditure for the formation of spores and their rapid dissemination, compared to the formation of sperm and carpogonium that give rise to the carposporophytic phase, which are only present when environmental conditions become adverse.

5. Epiphytism

The highest number of epiphytes was obtained in the dry season with 92, observing the highest number of species from the Rhodomelaceae, Wrangeliaceae and Ceramiaceae families with 11 each, most of these species are filamentous, small, and annual. Most of the epiphytes were found growing frequently on other larger Rhodophyta such as Gracilaria, Laurencia, Palisada, Acanthophora, Alsidium, and Digenea. It has been suggested that host longevity must be long enough to allow these organisms to complete their life cycle and that this could be a reason for the absence of epiphytes in algae with short and ephemeral lifecycles (Santelices 1977SANTELICES, B. 1977. Ecología de las algas marinas bentónicas. Universidad Católica de Chile. Santiago. 384 p.). Regarding the rainy season, 87 species were identified, a number very close to that found in the dry season. In this season it was observed that fleshy corticated macroalgae grew both on rocky substrates and epiphytes of other macroalgae, which can be attributed to the fact that the populations of both epilithic and epiphytic benthic marine algae are growing. On the other hand, it is necessary to consider that in the RBSK there are seagrass meadows and mangroves, both populations of vascular plants offer an adequate substrate for the fixation and growth of epiphytic algae (Nava-Olvera et al. 2017NAVA-OLVERA, R., MATEO-CID, L.E., MENDOZA-GONZÁLEZ, A.C. & GARCÍA-LÓPEZ, D.Y. 2017. Macroalgas, microalgas y cianobacterias epífitas del pasto marino Thalassia testudinum (Tracheophyta:Alismatales) en Veracruz y Quintana Roo, Atlántico mexicano. Rev. Biol. Mar. Oceanogr. 52(3):429–439., Peña-Salamanca 2017PEÑA-SALAMANCA, E. 2017. El complejo Bostrychietum: la flora de algas asociadas a las raíces del manglar en la costa pacífica colombiana. Revista Acad. Colomb. Ci. Exact. 41(160):338–348. doi: https://dx.doi.org/10.18257/raccefyn.485
https://doi.org/10.18257/raccefyn.485...
).

Seagrass meadows Thalassia testudinum represent a coastal ecosystem of great value in the RBSK, mainly due to the ecosystem services they offer, the vertical and horizontal structure of the seagrass plants favours the appearance of many microhabitats, transforming the leaves into an ideal substrate for the development of many epiphytic organisms (Díaz-Merlano et al. 2003DÍAZ-MERLANO, J.M., BARRIOS, L. & GÓMEZ-LÓPEZ, D. 2003. Las praderas de pastos marinos en Colombia: Estructura y distribución de un ecosistema estratégico, 160 p. INVEMAR, Serie Publicaciones Especiales 10, Santa Marta., Nava-Olvera et al. 2017NAVA-OLVERA, R., MATEO-CID, L.E., MENDOZA-GONZÁLEZ, A.C. & GARCÍA-LÓPEZ, D.Y. 2017. Macroalgas, microalgas y cianobacterias epífitas del pasto marino Thalassia testudinum (Tracheophyta:Alismatales) en Veracruz y Quintana Roo, Atlántico mexicano. Rev. Biol. Mar. Oceanogr. 52(3):429–439.). Nava-Olvera et al. (2017)NAVA-OLVERA, R., MATEO-CID, L.E., MENDOZA-GONZÁLEZ, A.C. & GARCÍA-LÓPEZ, D.Y. 2017. Macroalgas, microalgas y cianobacterias epífitas del pasto marino Thalassia testudinum (Tracheophyta:Alismatales) en Veracruz y Quintana Roo, Atlántico mexicano. Rev. Biol. Mar. Oceanogr. 52(3):429–439. in their study of epiphytic algae in Veracruz and Quintana Roo, determined 46 epiphytic algae taxa on T. testudinum in Santa Rosa, Quintana Roo, 38 of them correspond to Rhodophyta, which highlights its high contribution quantitatively compared to other groups of algae. This dominance is consistent with previous records in other regions, where red algae have been documented to dominate in species composition and biomass (Mendoza-González & Mateo-Cid 1992MENDOZA-GONZÁLEZ, A.C. & MATEO-CID, L.E. 1992. Algas marinas bentónicas de Isla Mujeres, Quintana Roo, México. Acta Bot. Mex. 19:37–61. DOI: https://doi. org/10.21829/abm19.1992.646.
https://doi.org/10.21829/abm19.1992.646...
, Quan-Young et al. 2006QUAN-YOUNG, L., DÍAZ-MARTÍN, M. & ESPINOZA-AVALOS, J. 2006. Algas epífitas de Bajo Pepito, Isla Mujeres, Quintana Roo, México. Rev. Biol. Trop. 54(2):317–328.). Records of Rhodophyta in studies of epiphytic floras, both in marine angiosperms (Ibarra-Obando & Aguilar-Rosas 1985IBARRA-OBANDO, S. & AGUILAR-ROSAS, R. 1985. Macroalgas flotantes y epífitas asociadas con Zostera marina L. en Bahía San Quintín (B.C., México) durante verano-otoño 1982: Biomasa y composición taxonómica. Cienc. Mar. 11:89–104., Barrios & Díaz 2005BARRIOS, J. & DÍAZ, O. 2005. Algas epífitas de Thalassia testudinum en el Parque Nacional Mochima, Venezuela. Bol. Centro Investig. Biol. 39:1–14.), and in macroalgae (Montañés et al. 2003MONTAÑÉS, M., REYES, J. & SANSÓN, M. 2003. La comunidad de epifitos de Zonaria tournefortii en el norte de Tenerife (Islas Canarias): análisis florístico y comentarios sobre su epifauna. Vieraea. 31:121–132., Quan-Young et al. 2006QUAN-YOUNG, L., DÍAZ-MARTÍN, M. & ESPINOZA-AVALOS, J. 2006. Algas epífitas de Bajo Pepito, Isla Mujeres, Quintana Roo, México. Rev. Biol. Trop. 54(2):317–328., Ortuño-Aguirre & Riosmena-Rodríguez 2007ORTUÑO-AGUIRRE, C. & RIOSMENA-RODRÍGUEZ, R. 2007. Dinámica del epifitismo en Padina concrescens (Dictyotales, Phaeophyta) en el sureste de la Península de Baja California, México. Cienc. Mar. 33:311–317.), point out that red algae are the group with the greatest specific richness within epiphytism, since they present life forms and reproductive strategies that allow them to remain longer in the phorophyte (Albis-Salas 2010ALBIS-SALAS, M.R. 2010. Características estructurales y fisiológicas de las praderas de Thalassia testudinum. Tesis de Maestría, Universidad Nacional de Colombia, Santa Marta.). Regarding mangroves, the roots and remains of these trees constitute a firm and safe substrate for the organisms that inhabit them; regarding epibiont algae and invertebrate communities, the roots provide a large moist surface available for colonization. It has been proven that the tolerance of mangrove algae to variations in salinity and periods of desiccation is due to their ability to synthesize, accumulate and regulate organic compounds that protect them from unfavourable factors for them (Ríos et al. 2019RÍOS, R., TEJADA, O.L., MORALES, D., MIRANDA, E. & CERRUD, A. 2019. Comunidad de algas del manglar de playa Estrella, isla Colón, Bocas del Toro, Panamá. REVMAR. 11(2):1–21.).

In our study, a total of 29 exclusive epiphytic species were located in mangrove roots and bark, mainly from the genus Bostrychia with 6 species, Caloglossa and Murrayella with one species each and Catenella 2. These results agree with what was recorded by other authors such as Peña-Salamanca (2017)PEÑA-SALAMANCA, E. 2017. El complejo Bostrychietum: la flora de algas asociadas a las raíces del manglar en la costa pacífica colombiana. Revista Acad. Colomb. Ci. Exact. 41(160):338–348. doi: https://dx.doi.org/10.18257/raccefyn.485
https://doi.org/10.18257/raccefyn.485...
and Ríos et al. (2019)RÍOS, R., TEJADA, O.L., MORALES, D., MIRANDA, E. & CERRUD, A. 2019. Comunidad de algas del manglar de playa Estrella, isla Colón, Bocas del Toro, Panamá. REVMAR. 11(2):1–21. who mention that the association of the Bostrychietum complex is well known, which is a group of algae associated with mangrove roots in tropical and subtropical areas, composed mainly of the genera Bostrychia, Caloglossa, Catenella, and Murrayella, as well as other genera. Epiphytes that were also found in the mangrove roots were Polysiphonia and Dasya with 5 taxa each and Chondria with 3, most of the species that make up the Bostrychietum algal complex such as the genera Polysiphonia, Dasya and Chondria they belong to the order Ceramiales which has the highest specific richness within Rhodophyta and its species have a wide worldwide distribution (Guiry & Guiry 2023GUIRY, M.D. & GUIRY, G.M. 2023. World-wide electronic Publication. National University of Ireland. Galway, Ireland. https://www.algaebase.org. (last access in 18/08/2023).
https://www.algaebase.org...
).

Conclusion

The analysis and integration of previous studies of Rhodophyta in the study area and the results obtained confirm the importance of carrying out phycofloristic inventories in little-worked coastal regions of the RBSK, which will result in a better understanding of the diversity of this important cluster. These results are the basis for future ecological, sustainable management and conservation studies, so it is recommended to continue with the sampling in the localities visited to observe the spatial and temporal changes of the flora that allow identifying possible alterations in the environmental conditions of the area of the RBSK.

Acknowledgments

We thank to the Instituto Politécnico Nacional for providing financial assistance, facilities, and equipment necessary for the development of this research. The Comisión de Operación y Fomento de Actividades Académicas del I.P.N. and EDI/IPN have provided fellowships to ACMG and LEMC. The authors wish to thank to Dirección General de Ordenamiento Pesquero y Acuícola de México for permission to collect in the restricted waters of the Biosphere Reserve of Sian Ka’an (No. DGOPA 08980.011111.3063).

Data Availability

Persistent identifier https://doi.org/10.15468/v7avng

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Publication Dates

  • Publication in this collection
    29 Apr 2024
  • Date of issue
    2024

History

  • Received
    09 Mar 2023
  • Accepted
    24 Mar 2024
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