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Article

Spatio-Temporal Variation in Cyanobacteria and Epiphytic Algae of Thalassia testudinum in Two Localities of Southern Quintana Roo, Mexico

by
Rocio Nava-Olvera
,
Luz Elena Mateo-Cid
,
Itzel González-Contreras
and
Ángela Catalina Mendoza-González
*
Instituto Politécnico Nacional, Escuela Nacional de Ciencias Biológicas, Departamento de Botánica, Laboratorio de Ficología, Carpio y Plan de Ayala, Colonia Santo Tomas, Ciudad de México 11340, Mexico
*
Author to whom correspondence should be addressed.
Diversity 2024, 16(6), 321; https://doi.org/10.3390/d16060321
Submission received: 13 April 2024 / Revised: 20 May 2024 / Accepted: 22 May 2024 / Published: 28 May 2024
(This article belongs to the Section Marine Diversity)
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Abstract

:
The leaves of Thalassia testudinum provide an ideal substrate for the establishment of small-sized algae with different morphologies that are abundant and diverse. There are few studies on epiphytism in Mexico, and most of them are floristic lists. The objective of this study was to analyze the taxonomic and morphofunctional composition of epiphytes in three climatic seasons, and their relationship with the phorophyte T. testudinum in two localities, El Uvero and Santa Rosa, in the south of Quintana Roo; three transects and fifteen quadrants were set in June and December (2014) and April (2015). A total of 84 epiphytic species were identified: 27 corresponded to Cyanobacteria, 10 to Phaeophyceae, 9 to Chlorophyta, and 38 to Rhodophyta. The highest specific richness was observed in Santa Rosa (73 species). The dry and summer rains seasons share a higher number of species compared to the winter rainy season. The crusty algae Hydrolithon farinosum was the dominant and most persistent species; in addition, filamentous algae presented great specific richness and coverage due to their morphology and reproductive strategies, which allowed them to successfully establish themselves on the phorophyte. This is related to the ecological succession of the epiphytes and seagrass phenology.

1. Introduction

Seagrass meadows are among the most productive ecosystems in the oligotrophic coastal waters of the Caribbean and are of great value to the biosphere, mainly due to the environmental services they provide [1,2]. In addition, seagrass meadows are heavily impacted by various natural phenomena and anthropic impacts in the region [3,4]. The turtle grass Thalassia testudinum K.D. Koenig is the most common and abundant seagrass species; it is also the main meadows former in the Mexican Caribbean [5,6], where many micro-habitats are formed. The abundance of micro-habitats allows for the establishment of great biological diversity with ecological, commercial, and conservation importance [1,2,7,8].
Particularly, the leaves of T. testudinum provide an ideal substrate for epiphytism [3,6,9], which is a lifestyle consisting of an organism using another plant as a substrate (a phorophyte) [10,11,12,13]. In the case of seaweed, epiphytism is an important ecological strategy since they obtain a substrate with optimal light conditions and adequate protection that allows their development [14]. Thus, in this environment, the composition of the seaweed community depends on its reproductive biology and dispersal capacity [7]. Furthermore, epiphytic algae are quite sensitive and quickly respond to changes in water quality [15,16].
The morphological, physiological, and ecological adaptations of cyanobacteria, microalgae, and macroalgae allow for their classification into morphofunctional groups (MFG) that are related to the level of disturbance in the environment, and they can be used as indicators of the environmental quality of ecosystems [17] along with the composition of algae communities and the abundance of each species of morphofunctional groups.
Studies of epiphytic algae in the Mexican Caribbean have mostly focused on taxonomic lists, such as those of Huerta-Múzquiz et al. [18], Mendoza-González and Mateo-Cid [19]; Mateo-Cid and Mendoza-González [20], Quan-Young et al. [21], Acosta-Calderón [22], and Hernández-Casas [23]. Research using the functional groups of algae and cyanobacteria for ecological studies is scarce [24,25,26,27].
The objective of the present work is to expand the taxonomic knowledge of the epiphytic algae and cyanobacteria of the seagrass T. testudinum; we sought to compare the epiphytism of two populations of T. testudinum from the Santa Rosa and El Uvero beaches in the climatic seasons of the Mexican Caribbean and to analyze the morphofunctional groups that would allow us to understand the temporal distribution of epiphytic algae.

2. Materials and Methods

2.1. Study Area

The study area was located on the southern coast of the state of Quintana Roo, Mexico. The two locations were El Uvero (18°57′26″ N 87°36′52″ W) and Santa Rosa (18°30′31″ N 87°45′32″ W), separated by 52 km (Figure 1). The study area was in the Tropical Cyclonic Zone of the Caribbean, with three climatic seasons: summer rains, winter rains, and dry season [28]. The area presents a climate Aw2(x′), which is warm sub-humid according to the Köppen classification modified by García [29] and Orellana et al. [30].
El Uvero beach, which is located 16 km south of the Sian Ka’an Biosphere Reserve and 26 km north of the Mahahual tourist complex, has a sandy–silty substrate. There are recreational activities on site, with a higher activity seen in April during the holiday season. Recreational activities include jet skis, inflatable toys, and devices placed on T. testudinum meadows, and there are also restaurant–bars and palapas. Santa Rosa Beach, located 1 km from the Xcalak Reefs National Park and 23 km south of Mahahual, has a compact sandy substrate. Near the T. testudinum meadow, there are human settlements dedicated to artisanal fishing. In both meadows, T. testudinum is dominant and associated with the seagrass Syringodium filiforme Kützing and macroalgae such as Halimeda spp. J.V. Lamouroux, Penicillus spp. Lamarck, Udotea spp. J.V. Lamouroux, and Avrainvillea spp. Decaisne.

2.2. Sampling Methods

Three samplings were performed, with one for each climatic season, in June 2014 (summer rains), December 2014 (winter rains), and April 2015 (dry season). Sampling was performed at low tide, from 0.5 to 2.0 m deep. At each sampling site, three 25 m transects were established along the meadow, positioned perpendicular to the coastline, and separated by 25 m. In turn, each transect had five 25 × 25 cm2 quadrants [31] placed along the transects spaced every five meters (n = 15 per site) (Figure 2). All T. testudinum leaves were collected from the pods using gardener hand shovels; they were fixed in 4% formalin in seawater. At the time of sampling, the air and water temperature were recorded in situ; salinity, dissolved oxygen, and ammonia concentrations were also measured using Hanna® Instruments Kits.

2.3. Isolation and Identification of Epiphytic Algae and Cyanobacteria

The epiphytic macroalgae were removed from the leaves of the phanerogam T. testudinum; the microalgae and cyanobacteria were obtained by scraping the plant sheets. Representatives of the Corallinaceae family were treated with 0.6 M HNO3 for decalcification. To observe the epiphytes, an Olympus® CX31RBSF binocular photonic microscope (Shenzhen, China) was used. The Bacillariophyta and Dinophyta were not considered in the present study because their processing requires specialized techniques and scanning electron microscopy, which were not the objective of this research.
Epiphytes classification was performed according to the work of Abbott and Hollenberg [32], Burrows [33], Cho et al. [34], Guimarães et al. [35], Littler and Littler [36], Schneider and Searles [37] Taylor [38], Hoek [39], and Won et al. [40]. The taxonomic determination of cyanobacteria was performed according to the work of Anagnostidis and Komárek [41,42,43,44,45,46]. The sequence of the taxonomic list followed the order proposed by Wynne [47] for Rhodophyta, Phaeophyceae, and Chlorophyta.
Nomenclatural updates were obtained from the taxonomic database AlgaeBase [48]. To characterize the functional groups, the classification of Steneck and Dethier [17] was used.
To determine the abundance dominance of epiphyte species on the surface of the sampled leaves, we used a modified scale (from 1 to 5) for phytobenthos based on Braun-Blanquet [49] and Boudouresque [50]. Five pods were chosen at random for each sampling unit, and the area covered by the epiphytes in the first 10 cm of the apical area of both sides of each leaf was determined using a ZEIGEN® stereoscopic microscope with squared Petri dishes.

2.4. Spatio-Temporal Analysis of the Species Composition of Epiphytic Algae

Significant differences were observed in abundance dominance by species between locations, seasons, and quadrants. A PERMANOVA and a non-metric multidimensional scaling analysis were performed to determine the distribution of epiphytic algae found on Thalassia by season and location.
We grouped the species present on T. testudinum by presence absence, locality (in Santa Rosa and El Uvero), and by climatic season (dry, winter rains, summer rains). Additionally, to compare the similarity of epiphytes between El Uvero and Santa Rosa, a cluster analysis was performed using the Jaccard index and the unweighted pair group method with arithmetic (UPGMA) clustering method.
To identify the variables that best characterize the abiotic environment of the two T. testudinum meadows, principal component analysis (PCA) was performed. From this information, a simple linear regression analysis was performed, correlating specific richness and depth.
Significant differences in abundance dominance by functional groups between locations, seasons, and quadrants were evaluated. A PERMANOVA and the relationship between variations in the abundance of epiphytic algae by functional groups and the environmental factors evaluated was estimated through a canonical correspondence analysis by season and localities. The data were transformed to log (x + 1) to unify the units. The statistical analysis was performed using the PAST v4.03 program [51].

3. Results

3.1. Species of Cyanobacteria and Epiphytic Algae

A total of 84 species of epiphytic algae and cyanobacteria were determined; 27 were Cyanobacteria, where 27 and 57 were epiphytic algae, and of these, 38 correspond to Rhodophyta, 9 to green algae, and 10 to brown algae (Table 1).

3.2. Specific Richess of Cyanobacteria and Epiphytic Algae for Locality

In total, 64 species were identified in the El Uvero meadow and 73 in Santa Rosa. The number of species present in both study sites was 53 (Table 1 and Table 2).

3.3. Specific Richness of Cyanobacteria and Epiphytic Algae by Climatic Seasons

The dry season had the highest epiphytic specific richness with 61 species; the rainy season had 53 species; and the winter rain season had the lowest number of species (37).
Rhodophyta was the best-represented group in the three seasons in both locations (Figure 3), followed by microalgae such as Aphanothece sp., Calothrix confervicola (Figure 4E), Entophysalis sp., and Trichocoleus polytrix. Phaeophyceae had the smallest number of species and was not found in the summer rainy season in both localities (Figure 3). The species T. polytrix and Bachelotia antillarum (Figure 4F) had the highest dominance abundance in the dry season in both localities (Table 1).
The PERMANOVA analysis showed significant differences in abundance dominance for species (p = 0.0026) between seasons, locations, and quadrants (Table 3). Thus, a non-metric multidimensional scaling analysis was performed to reflect the spatial and temporal relationships of the abundance dominance of epiphytic algae on T. testudinum; the analysis showed no grouping pattern between the sampling sites, which means that there were no significant differences between locations according to the abundance dominance of epiphytic algal species on T. testudinum (Figure 5).
In contrast, the PERMANOVA analysis by seasons showed that there was some grouping for the winter rainy season in both locations; this indicates that there are significant differences between climatic seasons in both locations.
In the cluster analysis, a similarity in species in both locations is observed in the dry and summer rains seasons; on the other hand, Santa Rosa in the dry season shows the highest dissimilarity with the previous groups (Figure 6).

3.3.1. Epiphytes and Environmental Variables

The specific environmental variables of the T. testudinum meadows (Table 4) used for principal components analysis indicate that the first three components explain 76.87% of the variance; PC1 explained 35.68% of the variance (eigenvalue 2.5) and PC2 23.95% (eigenvalue 1.68). PC1 represented a positive gradient related to dissolved oxygen and a negative gradient related to depth; PC2 showed a positive gradient related to water temperature and a negative gradient related to salinity.
Linear regression between depth and specific richness shows an inverse correlation (Figure 7).

3.3.2. Morphofunctional Groups of Epiphytes Algae

Six morphofunctional groups were located; 51% of the total epiphytes corresponded to the group of filamentous algae with 44 species, 27 species were microalgae, 8 corticate macrophytes, 2 foliose, 2 crustose, and 1 a calcareous articulated macrophyte. The composition of the functional groups by location was similar (Table 5).
In terms of the variation between climatic seasons, five functional groups were obtained for each climatic season, with variations in the group articulated as calcareous algae and foliose algae (Figure 8).
The group of crusty algae was composed of the same two species in the three seasons: Hydrolithon farinosum and Pneophyllum confervicola. The functional groups that presented the highest abundance dominance were filamentous algae (Figure 4B), microalgae, and crusty algae (Figure 4A).

3.4. Relationship between Functional Groups and Environmental Factors

The PERMANOVA analysis showed significant differences in functional groups (p = 0.0001) between seasons (Table 6). Regarding the relationship between the epiphytic algae found on Thalassia and the recorded environmental factors, the canonical correspondence analysis showed that the first two axes explained 86.07% of the variance in the data. Axis 1 explained 64.84% of the variance, mainly due to dissolved oxygen (−0.401), air temperature (−0.455), and salinity (0.404). Axis 2 explained 21.23% of the variance and was determined by water temperature (0.212) and depth (0.218) (Figure 9). On the other hand, microalgae (e.g., Figure 10A) and filamentous algae (e.g., Figure 4E,F and Figure 10B–D) were observed in the center of the graph (Figure 9) and were widely distributed between sites and seasons.

4. Discussion

4.1. Specific Richness

A higher number epiphytic algae species was found than those reported for the Mexican Caribbean by Mendoza-González and Mateo-Cid [19], Isla Mujeres Quan-Young [21], Santa Rosa, and Nava-Olvera et al. [27]; however, it is lower in comparison to other substrates, such as Digenea mexicana [23], and this is attributed to its cellular architecture and physiological aspects, highlighting why it is important to incorporate epiphytic algae into floristic lists as well as to carry out studies in other T. testudinum meadows, both in the Mexican Caribbean and in the Gulf of Mexico, as has already been proposed by several authors [52,53,54].
The best-represented taxonomic group of epiphytes algae was Rhodophyta (38 species), which highlights the high quantitative contribution of this group in contrast to other groups such as Phaeophyceae (Heterokontophyta), and Chlorophyta. These data agree with previous reports for other regions, where red algae reportedly dominate in composition and biomass [7,55]. Thus, the records of red algae in studies of epiphytic flora in various marine macrophytes are the most abundant, both in marine angiosperms [3,21,23,56] and different macroalgae [14,23,52,53,57,58]. Within the group of red algaes, the Rhodomelaceae family was the best represented in our study, just like other authors have described [14,52,58]. On the other hand, 14 species were determined in both localities (Table 2).
The results show significant differences in terms of abundance dominance between locations (Table 3). The cyanobacteria group presents a greater similarity between the species from both seasons, and within the epiphytic algae the phylum Rhodophyta show great similarity in comparation of others groups (Table 2).

4.2. Specific Richness and Abundance Dominance by Climatic Seasons

There is significant difference between climatic seasons in terms of abundance dominance; the winter rain season was different from the other seasons in terms of its composition of species (Figure 6) and abundance dominance (Table 3). We also found that the lowest number of epiphytic species was observed in the winter rain season (Table 1, Figure 3). The highest number of epiphytic species were observed in the dry season, which contrasts with reports by Mateo-Cid and Mendoza-González [20] and Mendoza-González and Mateo-Cid [19], who observed a lower number of species in the dry season. These differences could be attributed to the differences in the sampling methods used in the different climatic seasons.
The algae Cladosiphon zosterae (Figure 4C) was found among the strictly epiphytic species, as Mateo-Cid and collaborators reported in 1996 [59], and it was present at both locations only in the dry season.

4.3. Epiphytes and Environmental Variables

All algae and cyanobacteria were categorized as annual organisms. The highest abundance dominance of epiphytic algae on the phorophyte T. testudinum was observed in the dry season; 100% of the total coverage was present at 10 cm of the apical zone and filamentous algae predominated on the edges of the leaf in all sampling units (Figure 4B). In comparison to the other seasons, the dry season was characterized by a lower water depth, higher temperatures, and a higher coverage of Thalassia on the sandy substrate (reaching a maximum in summer) (Table 4), which are favorable conditions for epiphytic algae. In contrast, the winter rain season was characterized by a lower coverage of Thalassia. These results reveal a more abundant adhesion surface for the epiphytes, which is related to a higher density of the pods and environmental conditions that favor their permanence. This idea has been reported by Borowitzka et al. [55] and Carruthers [60], who mention that the light that penetrates the meadow canopy determines the load of epiphytes. In our present study, the visibility in the meadows was total at low tide, which means that the attenuation of light was only affected by the shading between the Thalassia leaves due to its density and the movement produced by the waves, and not for other factors.
Algae have physiological strategies for thriving, such as the presence of accessory pigments that capture light at different wavelengths. This is important in this microhabitat since light penetration decreases due to the shading from the leaves and allows for the development of groups of algae. The presence of accessory pigments allows them to establish and develop on the phorophyte. This physiological strategy causes competition for light availability, which is reflected in our sampling: in the apical layer of the leaves, there was a higher load of epiphytes, as this is where they would be under optimal light and protection conditions.
According to the analyses carried out, we have found that depth influences the distribution of epiphytes. The highest number of green algal species were observed at a shallow depth (<1 m). On the other hand, the presence of red algae and cyanobacteria along the depth gradient between 0.5 and 1.70 m makes these groups the best represented at a higher depth with a higher abundance dominance (>1 m depth); the flat morphology of some species, such as crusty algae, allow them to absorb a higher amount of light [61,62]. In keeping with this observation, it has been reported that the relative abundance of Rhodophyta increases with depth [63,64].

4.4. Morphofunctional Groups and Climatic Seasons

The microalgae and filamentous algae groups were widely distributed by site and season, and these groups were distinct from the other groups of algae according to the number of species. Microalgae establish themselves by forming a biofilm, which also allows for other algae to establish. Encrusting coralline algae were the group always present on T. testudinum leaves, thus making them the most important epiphyte, although with a low number of species, which is in keeping with previous reports [3,14,60,65,66]. From lowest to highest abundance dominance, Hydrolithon farinosum and Pneophyllum confervicola, respectively, were found in all T. testudinum leaves from the youngest to the most senescent (Figure 4A). Once these organisms become established, they persist throughout the lifespan of the substrate [55]. Among these encrusting algae, filamentous algae proliferate, as reported by Sebens [67] and Steneck [62]. The establishment and permanence successes of filamentous algae are due to the different reproductive structures that they form [68], but also to the fact that opportunistic eurotypic algae with a low degree of complexity and high biomass are typical of environments with high nutrient content, as they can easily take advantage of the nutrients in the environment, counteracting herbivory with high growth rates [17,68,69]; most of the species of red algae that predominated in the sporophytic phase belong to this group, which is also the most common according to previous studies [18,19,20,27,57]. This is because this type of asexual reproduction has the advantage of requiring less energy expenditure for the formation of spores, which are then quickly disseminated, allowing for efficient dispersion and a high probability of fixation and development of thalli [70]. We also observed species of the genera Gayliella, Herposiphonia, Lophosiphonia, and Polysiphonia on the same Thalassia leaf. These species presented various reproductive states including spermatangia, carposporangia (Figure 10C), and tetrasporangia, which allow for the life cycle of these species to be completed and for their continuous establishment on adjacent leaves due to the rate of leaf turnover.
It has been documented that the period of highest reproduction of T. testudinum in the Caribbean is from April to September [2]. In our sampling performed in April, an increase in epiphytes was observed, possibly due to the decrease in energy reserves that are necessary to produce the secondary compounds required for plant defense mechanisms, such as polyphenols, flavonoids, and fatty acids [71,72,73,74,75]. The decrease in energy reserves is possibly because the energetic investment of Thalassia destines its reproduction, which allows for the establishment of a higher load of epiphytes. Algae functional groups, or species with characteristics that allow them to compete for a substrate, will thus successfully establish themselves on the leaves.
From November to February, the absence of flowers and fruits in Thalassia probably reflects an energetic investment in defense against epiphytes, which coincides with the winter rain season. This contrasts with studies performed by [72], who found higher amounts of secondary metabolites in Thalassia in October (winter rain season). In this month, we found the lowest number of epiphytes and the presence of gametangia-type reproductive structures that require higher energy investment, in addition a higher filamentous biomass in the old leaves during flowering periods [76]. In addition to the low abundance dominance of algae in this period, crusty algae covered between 25% and 75% of the surface of the phorophyte, which suggests the existence of interactions in timescales between the longevity of the organism and the reproductive biology of the epiphytic algae, in addition to the synchrony between the phenology of the epiphytes and the phorophyte. This is reflected in an increase in the reproduction of epiphytes as the phorophyte ages [77], indicating a lower possibility of entry for new species since defense substances will prevent their fixation and establishment on the phorophyte. This contrasts with reports by various authors such as [78], who indicate that the colonization of epiphytes is mainly controlled by biological factors such as phorophyte growth and the life cycle of epiphytes.

5. Conclusions

In this study, the temporal variation in the epiphytic communities on T. testudinum was determined, and it was found to be related to the phenology of this phorophyte through morphological and physiological attributes and life strategies that allow epiphytes to reproduce, grow quickly, and establish themselves on the phorophyte through an ecological succession, as explained by the presence of functional groups. The importance of depth is also shown, relating to the light and shading produced by the leaves of T. testudinum, which determines the presence and development of epiphytes and their taxonomic and functional variation.
This work shows the importance of Thalassia as a good substrate for the establishment of epiphytes due to its variations in morphology and development throughout the year, which determine epiphyte load. Our work also highlights the presence of exclusive species on Thalassia, where the turnover of the leaves marks the dynamics of the community. The results presented here are the basis for subsequent studies, since they represent a preliminary vision of the epiphyte communities on seagrasses, especially on the coast of Quintana Roo. Due to the arrival of Sargassum in the years following the time of the study, it is necessary to analyze its effects on the epiphyte communities of seagrasses, highlighting not only the importance of characterizing and establishing specific functional groups of epiphytic algae in ecological studies but also the importance of considering other biotic and abiotic factors that can influence the establishment of epiphytic algae.

Author Contributions

Conceptualization, R.N.-O., L.E.M.-C. and Á.C.M.-G.; methodology, L.E.M.-C., Á.C.M.-G., R.N.-O. and I.G.-C.; validation, L.E.M.-C.; formal analysis, R.N.-O. and I.G.-C.; investigation, R.N.-O., L.E.M.-C., Á.C.M.-G. and I.G.-C.; resources, L.E.M.-C. and Á.C.M.-G.; writing-original draft preparation, R.N.-O.; writing-review and editing, R.N.-O. and L.E.M.-C.; visualization, R.N.-O. and L.E.M.-C.; supervision, L.E.M.-C. All authors have read and agreed to the published version of the manuscript.

Funding

This research received funding from the Instituto Politécnico Nacional for providing financial support, facilities, and necessary equipment for the development of this study through projects SIP-20150767, 20150850, 20161052, and 20164772.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Authors can provide data if required.

Acknowledgments

The first author thanks the National Council of Science, Humanities, and Technology (CONACHyT) for the scholarship awarded. The second and fourth authors are grateful for the scholarship awarded by the Commission for the Operation and Promotion of Academic Activities (COFAA) and the incentives from the Researchers’ Encouragement Program (EDI). Thanks to C. Mariana Hernández Casas, A. Gerardo Garduño, and Julio A. Acosta Calderón for their logistical support.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

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Figure 1. Location of the study area and sampling sites on the southern coast of Quintana Roo. El Uvero was located 16 km south from the Sian Ka’an Biosphere Reserve, and Santa Rosa was 1 km north from the Xcalak Reefs National Park; the Protected Natural Areas (ANP for its Spanish acronym) for the year 2014 are shaded.
Figure 1. Location of the study area and sampling sites on the southern coast of Quintana Roo. El Uvero was located 16 km south from the Sian Ka’an Biosphere Reserve, and Santa Rosa was 1 km north from the Xcalak Reefs National Park; the Protected Natural Areas (ANP for its Spanish acronym) for the year 2014 are shaded.
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Figure 2. Sampling at different depths at low tide: (A) low depth (B) greater depth.
Figure 2. Sampling at different depths at low tide: (A) low depth (B) greater depth.
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Figure 3. Seasonal variation in the specific richness of epiphytic algae determined on T. testudinum in El Uvero and Santa Rosa by taxonomic group. The best represented group in the three seasons and the two localities is Rhodophyta, whereas Phaeophyceae is not found in the summer rainy season in both localities.
Figure 3. Seasonal variation in the specific richness of epiphytic algae determined on T. testudinum in El Uvero and Santa Rosa by taxonomic group. The best represented group in the three seasons and the two localities is Rhodophyta, whereas Phaeophyceae is not found in the summer rainy season in both localities.
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Figure 4. Cyanobacteria and epiphytic algae on T. testudinum. (A) Surface view of the crusted algae (scale 15 mm). (B) Surface view of filamentous algae (Scale 15 mm). (C) Cladosiphon zosterae under a stereoscopic microscope (scale 0.5 mm). (D) Chondria polyrhiza under a stereoscopic microscope (scale 0.5 mm). (E) Cross-section of phorophyte with Calothrix confervicola (scale 50 μm). (F) Bachelotia antillarum filamentous algae (scale 50 μm).
Figure 4. Cyanobacteria and epiphytic algae on T. testudinum. (A) Surface view of the crusted algae (scale 15 mm). (B) Surface view of filamentous algae (Scale 15 mm). (C) Cladosiphon zosterae under a stereoscopic microscope (scale 0.5 mm). (D) Chondria polyrhiza under a stereoscopic microscope (scale 0.5 mm). (E) Cross-section of phorophyte with Calothrix confervicola (scale 50 μm). (F) Bachelotia antillarum filamentous algae (scale 50 μm).
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Figure 5. Non-metric multidimensional scaling analysis by season and location (Stress 0.1689, Bray–Curtis similarity), SRS: summer rain season, WRS: winter rain season, DS: dry season.
Figure 5. Non-metric multidimensional scaling analysis by season and location (Stress 0.1689, Bray–Curtis similarity), SRS: summer rain season, WRS: winter rain season, DS: dry season.
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Figure 6. Clustering of epiphytic algae using the UPGMA method and the Jaccard similarity index for El Uvero and Santa Rosa in the three climatic seasons, SRS: summer rain season, WRS: winter rain season, DS: dry season.
Figure 6. Clustering of epiphytic algae using the UPGMA method and the Jaccard similarity index for El Uvero and Santa Rosa in the three climatic seasons, SRS: summer rain season, WRS: winter rain season, DS: dry season.
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Figure 7. Linear regression analysis between depth and specific richness (r = −0.35, r2 = 0.12, t = −3.5, p = 5.4 × 10−4) with 95% confidence.
Figure 7. Linear regression analysis between depth and specific richness (r = −0.35, r2 = 0.12, t = −3.5, p = 5.4 × 10−4) with 95% confidence.
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Figure 8. Seasonal variation in the specific richness of epiphytic algae determined on T. testudinum in El Uvero and Santa Rosa by morphofunctional group.
Figure 8. Seasonal variation in the specific richness of epiphytic algae determined on T. testudinum in El Uvero and Santa Rosa by morphofunctional group.
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Figure 9. Analysis of canonical correspondences between environmental variables and the abundance of epiphytic algae by morphofunctional groups, the black dots represent winter rains, the blue dots are summer rains, and the red dots represent the dry season.
Figure 9. Analysis of canonical correspondences between environmental variables and the abundance of epiphytic algae by morphofunctional groups, the black dots represent winter rains, the blue dots are summer rains, and the red dots represent the dry season.
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Figure 10. Cyanobacteria and epiphytic algae on T. testudinum. (A) Chroococcus turgidus (scale 4.8 μm). (B1) Lophosiphonia cristata (scale 112.5 μm); (B2) cross-section of the filament of L. cristata where 10 pericentrals are observed (scale 16 μm). (C) Polysiphonia scopulorum with cystocarps (scale 41 μm). (D1,D2) Rivularia bornetiana, (D1) base approach, its heterocyst is observed (scale 31.7 μm), (D2) filamentous portion (scale 111 μm).
Figure 10. Cyanobacteria and epiphytic algae on T. testudinum. (A) Chroococcus turgidus (scale 4.8 μm). (B1) Lophosiphonia cristata (scale 112.5 μm); (B2) cross-section of the filament of L. cristata where 10 pericentrals are observed (scale 16 μm). (C) Polysiphonia scopulorum with cystocarps (scale 41 μm). (D1,D2) Rivularia bornetiana, (D1) base approach, its heterocyst is observed (scale 31.7 μm), (D2) filamentous portion (scale 111 μm).
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Table 1. List of cyanobacteria and epiphytic algae in El Uvero and Santa Rosa by family of every group taxonomic. The abundance dominance value is indicated by location, climatic season, morphofunctional groups, and reproductive structures. Climatic season: SRS: summer rain season, WRS: winter rain season, DS: dry season. GMF: morphofunctional group. I. microalgae, II. filamentous algae, III. foliose algae, IV. corticated macrophytes, V. articulated calcareous algae, VI. crustose algae. RS: reproductive structures, Tr = tetrasporangia, Pl = plurangia, Ht = heterocysts, Hm = hormogonium, Mn = monosporangia, Ga = gametangia; Og = oogonium, ♀ = cystocarp/gonimoblast, ♂ = spermatia and, Ve = vegetative. Abundance dominance: 1. less than 5%; 2. between 5% and 25%; 3. between 25% and 50%; 4. between 50% and 75%; 5. greater than 75% of the surface covered by epiphytes.
Table 1. List of cyanobacteria and epiphytic algae in El Uvero and Santa Rosa by family of every group taxonomic. The abundance dominance value is indicated by location, climatic season, morphofunctional groups, and reproductive structures. Climatic season: SRS: summer rain season, WRS: winter rain season, DS: dry season. GMF: morphofunctional group. I. microalgae, II. filamentous algae, III. foliose algae, IV. corticated macrophytes, V. articulated calcareous algae, VI. crustose algae. RS: reproductive structures, Tr = tetrasporangia, Pl = plurangia, Ht = heterocysts, Hm = hormogonium, Mn = monosporangia, Ga = gametangia; Og = oogonium, ♀ = cystocarp/gonimoblast, ♂ = spermatia and, Ve = vegetative. Abundance dominance: 1. less than 5%; 2. between 5% and 25%; 3. between 25% and 50%; 4. between 50% and 75%; 5. greater than 75% of the surface covered by epiphytes.
EL UVEROSANTA ROSA
TAXAFMGSRSWRSDSSRSWRSDSRS
CYANOBACTERIA
Microcystaceae
1. Aphanothece sp.I111111Ve
Entophysalidaceae
2. Entophysalis sp.I111111Ve
Chroococcaceae
3. Chroococcus turgidus (Kützing) NägeliI1-11--Ve
Gomphosphaeriaceae
4. Gomphosphaeria salina Komárek and HindákI1-----Ve
Hyellaceae
5. Cyanoderma lineare (Setchell and N.L. Gardner) Komárek and AnagnostidisI1--1--Ve
Coleofasciculaceae
6. Coleofasciculus chthonoplastes (Gomont) M. Siegesmund, J.R. Johansen and T. FriedlI1111-1Hm
7. Stanieria sublitoralis (A.Lindstedt) Anagnostidis and PantazidouI 1Ve
Leptolyngbyaceae
8. Leptolyngbya ectocarpi (Gomont) Anagnostidis and KomárekI-1--11Ve
9. L. jadertina (Kützing ex Hansgirg) AnagnostidisI1-----Ve
10. Trichocoleus polythrix (Forti) AnagnostidisI114114Ve
Cyanothecaceae
11. Cyanothece halobia Roussomoustakaki and AnagnostidisI1113-1Ve
Oscillatoriaceae
12. Lyngbya aestuarii Liebman ex GomontI111--1Ve
13. L. confervoides C. Agardh ex GomontI131-11Ve
14. L. majuscula Harvey ex GomontI--1---Ve
15. Oscillatoria funiformis (Vouk) KomárekI1-1111Ve
Spirulinaceae
16. Spirulina major Kützing ex GomontI---1--Ve
17. S. meneghiniana Zanardini ex GomontI-1---1Ve
18. S. robusta H. WelshI--1--1Ve
19. S. subsalsa Oersted ex GomontI--11-1Ve
Rivulariaceae
20. Calothrix confervicola C. Agardh ex Bornet and FlahaultI111311Ht
21. C. contarenii Bornet and FlahaultI--1211Ht
22. C. fuscoviolacea P. Crouan and H. Crouan ex Bornet and FlahaultI1--11-Ht
23. C. pulvinata C. Agardh ex Bornet and FlahaultI---1--Ht
24. Scytonematopsis crustacea (Thuret ex Bornet and Flahault) Kováčik and KomárekI---1--Ht
25. Dichothrix sp.I---- 1Ht
26. Dichothrix ramenskii ElenkinI--11-1Ht
27. Rivularia bornetiana SetchellI--1--1Ht
RHODOPHYTA
Colaconemataceae
28. Colaconema dasyae (Collins) Stegenga, I. Mol, Prud’homme and LokhorstII111--1Mn
29. C. hallandicum (Kylin) Afonso-Carillo, Sanson, Sangil and Díaz-VillaII1----1Mn
30. C. robustum (Børgesen) Huisman and WoelkerlingII1-1--1Mn
31. C. savianum (Meneghini) R. NielsenII1-1--1Mn
Corallinaceae
32. Jania capillacea HarveyV1----2Ve
33. Pneophyllum confervicola (Kützing) Y.M. ChamberlainVI533554Tr
Hydrolithaceae
34. Hydrolithon farinosum (J.V. Lamouroux) Penrose and Y.M. ChamberlainVI533554Tr
Callithamniaceae
35. Crouania attenuata (C. Agardh) J. AgardhII-----1Ve
36. Crouanophycus latiaxis (I.A. Abbott) A. AthanasiadisII1/1----1Ve
Ceramiaceae
37. Centroceras gasparrini (Meneghini) KützingII -2--2♂
38. Ceramium brevizonatum H.E. PetersenII1--1--Tr
39. C. cimbricum f. flaccidum (H.E. Petersen) G. Furnari and D. SerioII----1-Tr
40. C. cruciatum Collins and HerveyII-----1Tr
41. C. luetzelburgii O.C. SchmidtII1-3111Tr
42. Gayliella flaccida (Harvey ex Kützing) T.O. Cho and L.M. McIvorII--1---Tr
43. G. transversalis (Collins and Hervey) T.O. Cho and FredericqII111111Tr
Wrangeliaceae
44. Anotrichium barbatum NägeliII2--1--
45. A. secundum (Harvey ex J. Agardh) G. FurnariII-----1Tr
46. A. tenue (C. Agardh) NägeliII1--2--Tr
47. Griffithsia radicans KützingII---1--Tr
Rhodomelaceae
48. Chondria curvilineata Collins and HerveyIV--2---Tr
49. Ch. polyrhiza Collins and HerveyIV2-21-1♂
50. Ch. pygmaea Garbary and VandermeulenIV211222Tr ♂
51. Herposiphonia secunda (C. Agardh) AmbronnII121111Tr ♀♂
52. Laurencia caduciramulosa Masuda and S. KawaguchiIV-----2♂
53. L. laurahuertana Mateo-Cid, Mendoza-González, Senties and Diaz-LarreaIV--2---Tr
54. Laurencia minuta Vandermeulen, Garbary and GuiryIV11----Tr ♀♂
54. L. obtusa (Hudson) J. V. LamourouxIV----2-Tr
56. Lophosiphonia cristata FalkenbergII1--1--♀♂
57. L. obscura (C. Agardh) FalkenbergII1-11-1♀♂
58. Melanothamnus gorgoniae (Harvey) Díaz-Tapia and MaggsII1-11-1Tr
59. Polysiphonia atlantica Kapraun and J.N. NorrisII1-----Tr♂
60. P. binneyi HarveyII--4---Tr♀
61. P. scopulorum HarveyII2-51-1Tr♀♂
Champiaceae
62. Champia parvula (C. Agardh) HarveyIV--2221Tr♀
Erythrotrichiaceae
63. Erythrotrichia carnea (Dillwyn) J. AgardhII1111-1Ve
Stylonemataceae
64. Chroodactylon ornatum (C. Agardh) BassonII1111-1Ve
65. Stylonema alsidii (Zanardini) K.M. DrewII1-11-1Ve
HETEROKONTOPHYTA
Acinetosporaceae
66. Feldmannia mitchelliae (Harvey) H.S. KimII--1-14Pl
Ectocarpaceae
67. Ectocarpus siliculosus (Dillwyn) LyngbyeII-----1Pl
Chordariaceae
68. Cladosiphon zosterae (J. Agardh) KylinII--2--2Un
69. Hecatonema floridanum (W.R. Taylor) W. R. TaylorII--1--1Pl
70. Myrionema strangulans GrevilleII-3----Pl
Bachelotiaceae
71. Bachelotia antillarum (Grunow) GerloffII--3-13Ve
Dictyotaceae
72. Canistrocarpus cervicornis (Kützing) De Paula and De ClerckIII----1-Ve
73. Dictyota pinnatifida. KützingIII----1-Ve
Sphacelariaceae
74. Sphacelaria rigidula KützingII-----1Pp
75. S. tribuloides MeneghiniII----1-Pp
CHLOROPHYTA
Phaeophilaceae
76. Phaeophila dendroides (P. Crouan and H. Crouan) BattersII112121Ve
Ulvellaceae
77. Ulvella lens P. Crouan and H. CrouanII111-11Ve
78. U. viridis (Reinke) R. Nielsen, C.J. O’Kelly and B. WysorII-11---Ve
Cladophoraceae
79. Cladophora albida (Nees) KützingII--3---Ve
80. C. liniformis KützingII111111Ve
81. Willeella brachyclados (Montagne) M.J. WynneII1----1Ve
Udoteaceae
82. Boodleopsis pusilla (Collins) W.R. Taylor, A.B. Joly and BernatowiczII---11-Ga
83. B. vaucherioidea Calderón-Sáenz and SchnetterII---11-Ve
84. B. verticillata E.Y. DawsonII---1--Ve
Table 2. Specific richness and diversity β of cyanobacteria and epiphytic algae in El Uvero and Santa Rosa for Taxa.
Table 2. Specific richness and diversity β of cyanobacteria and epiphytic algae in El Uvero and Santa Rosa for Taxa.
TaxaEl UveroSanta RosaDiversity β
Jaccard Index
Cyanobacteria22240.74
Algae
   Rhodophyta31330.68
   Chlorophyta670.44
   Phaeophyceae590.4
Total species64730.63
Table 3. Multivariate analysis by permutations (PERMANOVA) of two factors of cyanobacteria and epiphytic algae (abundance dominance) in Thalassia testudinum between seasons and localities (permutation N: 9999).
Table 3. Multivariate analysis by permutations (PERMANOVA) of two factors of cyanobacteria and epiphytic algae (abundance dominance) in Thalassia testudinum between seasons and localities (permutation N: 9999).
Sources of VariationSum of SquaresDfMean SquareFp
Locality0.2867210.286722.72130.0203
Season1.403820.701926.6620.0001
Interaction1.327920.663956.30160.0001
Residual8.8503840.10536
Total11.86989
Table 4. Average variation (±standard deviation) by climatic season of the environmental variables measured in El Uvero and Santa Rosa.
Table 4. Average variation (±standard deviation) by climatic season of the environmental variables measured in El Uvero and Santa Rosa.
El UveroSanta Rosa
VariableSummer RainsWinter RainsDrySummer RainsWinter RainsDry
Salinity (g/kg)36 ± 0.0839.1 ± 0.08437.43 ± 0.2334.5 ± 0.4240 ± 035.6 ± 0.59
Dissolved oxygen (mg/L)6.1 ± 0.847.1 ± 0.0847.98 ± 0.136.37 ± 0.124.7 ± 0.257.4 ± 0.15
Air temperature(°C)28.87 ± 1.0528.2 ± 0.5629.6 ± 0.8329 ± 0.6724.73 ± 0.4628 ± 0.93
Water temperature(°C)30.17 ± 0.5928.99 ± 0.2728.3 ± 0.5330.27 ± 0.728.67 ± 0.4928.27 ± 1.03
Depth (cm)0.71 ± 0.130.59 ± 0.270.7 ± 0.281.15 ± 0.291.21 ± 0.320.6 ± 0.38
Ammonia (mg/L)0.50.510.50.51
Coverage of Thalassia0.3 ± 0.1635.33 ± 12.7435.33 ± 41.3914.87 ± 12.4727.6 ± 22.862.73 ± 39.16
Number of Thalassia pods16.87 ± 6.7214.2 ± 5.4410.73 ± 14.917.13 ± 11.116.6 ± 19.422.67 ± 12.5
Table 5. Morphofunctional groups by climatic season.
Table 5. Morphofunctional groups by climatic season.
Morphofunctional GroupsSummer RainsWinter RainsDry
I. Microalgae201320
II. Filamentous algae261732
III. Foliose algae020
IV. Corticated macrophytes436
V. Articulated calcareous algae101
VI. Crustose algae222
533761
Table 6. Multivariate analysis by permutations (PERMANOVA) of two factors of species richness by functional groups of cyanobacteria and epiphytic algae in Thalassia testudinum between seasons and localities (permutation N: 9999).
Table 6. Multivariate analysis by permutations (PERMANOVA) of two factors of species richness by functional groups of cyanobacteria and epiphytic algae in Thalassia testudinum between seasons and localities (permutation N: 9999).
Sum of SquaresdfMean SquareFp
Locality0.090010.090051.39820.1938
Season2.248921.124417.4590.0001
Interaction−0.19272−0.09636−1.49630.1281
Residual4.5084700.06440
Total6.654675
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Nava-Olvera, R.; Mateo-Cid, L.E.; González-Contreras, I.; Mendoza-González, Á.C. Spatio-Temporal Variation in Cyanobacteria and Epiphytic Algae of Thalassia testudinum in Two Localities of Southern Quintana Roo, Mexico. Diversity 2024, 16, 321. https://doi.org/10.3390/d16060321

AMA Style

Nava-Olvera R, Mateo-Cid LE, González-Contreras I, Mendoza-González ÁC. Spatio-Temporal Variation in Cyanobacteria and Epiphytic Algae of Thalassia testudinum in Two Localities of Southern Quintana Roo, Mexico. Diversity. 2024; 16(6):321. https://doi.org/10.3390/d16060321

Chicago/Turabian Style

Nava-Olvera, Rocio, Luz Elena Mateo-Cid, Itzel González-Contreras, and Ángela Catalina Mendoza-González. 2024. "Spatio-Temporal Variation in Cyanobacteria and Epiphytic Algae of Thalassia testudinum in Two Localities of Southern Quintana Roo, Mexico" Diversity 16, no. 6: 321. https://doi.org/10.3390/d16060321

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