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Article

Spatio-Temporal Structure of Two Seaweeds Communities in Campeche, Mexico

by
Cynthia Mariana Hernández-Casas
,
Ángela Catalina Mendoza-González
,
Deisy Yazmín García-López
and
Luz Elena Mateo-Cid
*
Instituto Politécnico Nacional, Escuela Nacional de Ciencias Biológicas, Departamento de Botánica, Laboratorio de Ficología, Carpio y Plan de Ayala, Colonia Santo Tomás, Mexico City 11340, Mexico
*
Author to whom correspondence should be addressed.
Diversity 2024, 16(6), 344; https://doi.org/10.3390/d16060344
Submission received: 13 April 2024 / Revised: 1 June 2024 / Accepted: 7 June 2024 / Published: 14 June 2024
(This article belongs to the Special Issue Ecology and Biogeography of Marine Benthos)
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Abstract

:
Macroalgae populations are influenced by various factors that define their spatial and temporal distribution in different habitats and regions. In Mexico, studies addressing the abundance and diversity of macroalgae communities related to environmental factors are scarce. The objective is to determine the spatio-temporal variation of the structure of the community of seaweeds in Xpicob and Villamar, Campeche, during three climatic seasons. Sampling took place during each season using transects and quadrants; additionally, the type of substrate, water temperature, transparency, depth, salinity, and dissolved oxygen, were recorded. The total richness was 74 taxa, corresponding to three classes: Phaeophyceae (3), Florideophyceae (36), and Ulvophyceae (35). Filamentous algae dominate in species richness in the intertidal zone at low depths, while fleshy and calcareous algae predominate in number and biomass in the subtidal zone at higher depths (60–200 cm). Twenty-eight species were common to both sites; meanwhile, 46 taxa were exclusive of specific sites, including 13 found exclusively in Xpicob and 33 in Villamar. The most favorable climatic season for the macroalgae located in Xpicob was the winter rain. For the macroalgae community in Villamar, the most favorable climatic season was the dry. These differences are likely attributed to the predominant environmental and physicochemical characteristics of each site.

1. Introduction

On the littoral of Campeche, studies of macroalgae have mostly been floristic in approach, for example: Huerta-Múzquiz and Garza-Barrientos (1966) [1] published one of the first works carried out in the Campeche area, specifically, for the Terminus Lagoon; 20 years later, Huerta-Múzquiz et al. (1987) [2] carried out a floristic study in the Yucatan Peninsula, in which 102 species were recorded for the Campeche coast; on the other hand, Ortega (1995) [3] obtained 80 species collected between 1964 and 1966 in the Laguna de Terminos. Callejas-Jiménez et al. (2005) [4] obtained 51 species from Santa Rosalía and Playa Preciosa, including 19 new records. Mateo-Cid et al. (2013) [5] listed 211 taxa of benthic algae from the Campeche coast, while Mendoza-González et al. (2013) [6] determined 85 species (74 macroalgae) associated with wrecks and other subtidal structures on the coast of Campeche. The information obtained in this specialized literature shows that the total number of marine algae for the Campeche coast is 271.
Regarding ecological studies of the Campeche coast, there is only the work carried out by Ortiz-Rosales (1988) [7], who, in his master’s thesis, obtained a total of 47 species; in addition, he observed that the substrate and the depth are the factors that have the greatest influence on the distribution, composition, and richness of benthic algae. Biodiversity and marine ecosystems are intrinsically linked to a wide range of services that are essential for sustainable development; the ecological characterization of communities is a fundamental part of the use and exploitation of resources, including seaweed.
Among the biological factors that significantly influence the establishment of macroalgae at specific ecological niches are their physiology, morphology, life cycle, development, and the permanence of the algae in their habitat. The study of these phenological and demographic events allows us to partially understand the ecology of algae species [8,9,10,11]. To characterize algae communities, biogeographic affinity and epiphytism are also used, which allow us to understand an important part of the dynamics of species succession [12,13,14,15].
Benthic marine macroalgae communities are exposed to the influence of various physical factors both on a global and local scale; among these, there are physical factors, such as the type of substrate and its availability, temperature, exposure to waves, and depth (related to light availability); and also chemical factors such as salinity, nutrient availability, acidity, and dissolved oxygen [10,11,16,17,18,19].
The main factor influencing the geographical distribution of algae is the temperature. In addition, the salinity, tidal waves, and type of substrate are factors that have the highest influence on the local distribution of algae [20]. Therefore, these abiotic factors, together with the biotic ones, are thought to be responsible for the seasonal variation of algae in a specific region, affecting the composition of the species and, therefore, the structure of algal communities [21]. The effects of these biotic and abiotic factors have been observed in various populations of algae, affecting not only their presence or absence but also their morphology [22,23].
Ecological studies allow us to know the dynamics of the structure of a community over a period. Thus, this study will provide updated information about the attributes of the macroalgal communities of Campeche and their association with abiotic factors, as well as their behavior throughout the different seasons, allowing to strengthen conservation proposals, as well as the potential use of this resource in the study area.

2. Materials and Methods

The collection of biological material was performed in two locations on the coast of Campeche. Xpicob is located at the coordinates 19°43′13″ N and 90°40′09″ W. Due to its proximity to a turtle camp with the same name, Xpicob is a community dedicated mostly to fishing, with a smaller part dedicated to ecotourism. In Xpicob, the sandy substrate predominates with scattered rocky aggregates. Villamar is located 83 km northeast of Laguna de Terminos at the coordinates 19°16′13″ N and 90°47′54″ W; it is a sandy beach located very close to the Aak-bal hotel complex, with rocky platforms, rocky aggregates, and Thalassia testudinum meadows (Figure 1).
According to the Köppen classification modified by García (2004) [24], the Campeche coastline has a variety of climates from very hot and warm semi-dry (BS1(h′)w(i′) and BS0(h′)w″(x′)) to the warm subhumid (Aw0(i′)gw″) and warm humid (Am), specifically, in the study locations, the warm subhumid occurs [24,25].

2.1. Fieldwork

At each location, three samplings were performed during October 2016 (winter rain season), April (dry season), and July 2017 (summer rain season).
Three 25 m transects were placed perpendicular to the coastline, separated by 25 m. Geographical coordinates of each transect were taken with an eXplorist 210 GPS Magellan® (Paris, France). A sampling unit consisted of 25 × 25 cm squares (0.0625 cm2) placed every five meters on the transect [26,27,28].
For each square, the following data were recorded: type of substrate, water temperature (using a 100 °C mercury thermometer), transparency (using a Secchi disk), depth (using a depth meter), salinity (using a Hanna HI3835 Kit (Hanna Instruments®, Mexico City, Mexico), and dissolved oxygen (using a Hanna HI3810 kit).
The macroalgae located in each square were detached from the substrate and placed in transparent plastic bags, previously labeled with the name of the location, date of collection, transect, and quadrant number, as well as the name of the people who performed the collection. Algae were subsequently fixed with 5% formalin seawater and transferred to the Phycology laboratory of the Escuela Nacional de Ciencias Biológicas.

2.2. Laboratory Work

The identification of algae species was performed using the keys and descriptions of various relevant references [29,30,31,32,33].
The calculation of dry biomass of each species was estimated by placing each specimen for 15 days under a botanical press. Specimens were subsequently weighed on an analytical balance (Ohaus Scout® model H-7294, with 1 g precision, ULINE MX, Nuevo Leon, Mexico). The dry biomass value was extrapolated to m2.
All epiphytic macroalgae were completely detached from their substrate before species determination and recording of biomass data.
Finally, each specimen was mounted on herbarium paper and added to the Phycological Collection of the Herbarium of the Escuela Nacional de Ciencias Biológicas (ENCB) of the IPN.

2.3. Species Composition

A floristic list of the marine macroalgae species located at both locations in the three sampling periods was prepared. The family, genera, and species were ordered according to the systematic criterion proposed by Wynne (2022) [34], while the nomenclatural update follows the scheme of Guiry and Guiry (2024) [35].

2.4. Biogeographic Affinity

Based on the floristic list observed, the biogeographic affinity was calculated using the Cheney index (1997) [36]: (R + C)/P, where R is the number of Rhodophyta species, C is the number of Chlorophyta species, and P is the number of Phaeophyceae species. Values > 6 indicate flora with tropical affinity, values < 3 indicate flora with temperate-cold affinity, and intermediate values indicate a mixed-type flora.

2.5. Distribution Profiles

With the data on the number of species per location and season, macroalgae distribution profiles were prepared along the beach, according to the variation of depth in the 25 m transect.

2.6. Temporal and Spatial Variation of Biomass

For both locations, the values of season–species biomass, total temporal biomass, temporal relative abundance, total species biomass, total annual biomass, and annual relative abundance were calculated using the formulas of Águila-Ramírez (1998) [37] shown below.
Specific temporality biomass (STB):
∑ i = 1 15 B i o m a s s   o f   s p e c i e s   n   i n   e a c h   q u a d r a n t ,   f o r   e a c h   t r a n s e c t   f o r   s e a s o n   k
Total temporality biomass (TTB):
∑ j = 1 S S p e c i f i c   t e m p o r a r y   b i o m a s s   f o r   e a c h   s e a s o n   f r o m   a l l   s p e c i e s
Temporal relative abundance (TRA): T R A = S T B T T B × 100
Total species biomass (TSB): T S B = ∑ K = 1 3 S T B
Total annual biomass (TAB): TAB = ∑ j = 1 S T T B   o f   t h e   t h r e e   s e a s o n s   o f   t h e   y e a r
Annual relative abundance (ARA): ARA = T S B T A B × 100
To determine if there were significant differences in biomass between locations or between seasons, a two-way PERMANOVA was applied using the Bray–Curtis similarity index, followed by a two-way ANOVA to identify which transects and/or squares were different according to their location or season.
In addition, to evaluate how similar the seasons and/or locations were in terms of biomass, the total biomass data of each species in each season (by location) were used to perform a grouping analysis (Cluster) using UPGMA (average linkage) and a Bray–Curtis matrix.

2.7. Index of Macroalgae Importance Value

Subsequently, the importance of the macroalgae species was determined according to the Importance Value Index (IVI), which correlates the biomass to the frequency of occurrence of a species [38] modified by [39], thus indicating the relative ecological importance of the species in a community.
I V I = R B i + R F i
where RF = R B = B i ∑ B i F i ∑ F i .
Bi is the biomass of each species of macroalgae, Fi is the proportion of each macroalgal species found in all quadrants.

2.8. Macroalgal Community Attributes

2.8.1. α (Alpha) Diversity

The spatial and temporal variation of community attributes (diversity, dominance, and evenness) was analyzed using the biomass data observed previously.
The α diversity for each season, at each location, was calculated using the Shannon–Wiener index. This index considers the fact that individuals are randomly sampled from an infinite population, and it is assumed that all species are represented in the sample [40].
H ′ = − ∑ i = 1 s p i l o g 2 p i
where H′ is the Shannon-Wiener index, p is ni/N, log2 is the base 2 logarithm, ni is the biomass in g/m2 of each species, N is the total biomass of macroalgae, and S is the number of species.

2.8.2. β (Beta) Diversity

Spatial β-diversity (Xpicob and Villamar) was calculated in terms of macroalgal species turnover using the Whittaker index [41].
B w = s α − 1
Similarly, to analyze the rate of change of algal communities over time, β diversity was analyzed on a temporal scale (winter rain, summer rain, and dry seasons). All statistical analyses were performed using the PAST 3.1 program [42].

2.8.3. Evenness Index

The distribution of the biomass of individuals between species was determined using the Pielou index (J′) or Evenness index [43]. These indices assumes that all species in the community have been considered in the sample [40].
J ′ = H ′ H ′ m a x ,
where J′ is the Pielou Evenness index, H′ is the Shannon-Wiener diversity index, H′max is the maximum value reached by H′ (H′max = log2 S), and S is the total number of species recorded.

2.8.4. Dominance Index

The indices that are based on dominance are generally inverse to the uniformity or evenness of the community; they only consider the representativeness of the species with the highest importance value without evaluating the contribution of the rest of the species. The Simpson index is strongly influenced by the importance of the most dominant species [40,44]. In the present work, this index was used to determine the dominance of the species with the following formula:
λ = ∑ p i 2
where pi is the proportional abundance of species i; that is, the biomass of species i divided by the total biomass of the species in the sample.

2.8.5. Relationship between Environmental Variables and Species Abundance

First, to determine if there were differences in environmental variables, between seasons or between sampling locations, a two-way PERMANOVA analysis was applied using the Bray–Curtis similarity index. Likewise, a two-way ANOVA was performed for each of the specific environmental variables (type of substrate, water temperature, transparency, salinity, dissolved oxygen, and depth) recorded in the field.
To test if there is a relationship between the biomass (abundance) of the species and the environmental variables, a Canonical Correspondence Analysis (CCA) was used, using seven environmental variables: salinity, temperature, depth, transparency, dissolved oxygen, and substrate (sandy/rocky). A value of 1 was assigned to the substrate that dominated in the quadrant, and 0 to the one that was not dominant. Because the environmental variables have different units, they were standardized with (ln X + 1) before performing the CCA. The CCA was performed using the XLSTAT V2019.3.2 program.

3. Results

3.1. Species Composition of the Algae Communities

A total of 74 taxa were identified (Table 1). The class Florideophyceae was the best represented, in terms of richness, with 36 species, followed by Ulvophyceae with 35 species, and Phaeophyceae with three. Table 1 also shows the turnover of species in terms of presence/absence throughout the three seasons at each location. It should be noted that part of the material listed below has already been morphologically and molecularly characterized, as is the case with the Udotea specimens [45] and Codiophyllum [46].

3.2. Biogeographic Affinity

The value of the Cheney index observed in this study was 23.6, which indicates that the flora of Campeche is tropical (Cheney > 6).

3.3. Spatial and Temporal Variation of Species Richness

The Florideophyceae class was the one with the highest species richness at both locations; however, Villamar had a higher species richness, with 61 taxa relative to Xpicob, where 41 species were identified (Figure 2).
The highest richness was observed in the dry season (58), followed by the summer rain (34) and winter rain seasons (34). During the winter rain and dry seasons, Florideophyceae was the class with the highest richness, with 20 and 29 species, respectively. In the summer rain season, the class with the highest richness was Ulvophyceae (19). Both Florideophyceae and Ulvophyceae had their highest richness during the dry season, with 29 and 26 species, respectively, and their lowest richness during the summer rain and winter rain seasons, with 17 and 13 species, respectively (Figure 3).
In the winter rain season, the highest richness was observed in Xpicob, with 25 species (only one more species than in Villamar); however, in the dry and summer rain seasons, Villamar recorded the highest richness, with 31 and 46 species, respectively (Figure 3).
Xpicob, in the winter rain season, presented two exclusive taxa, Cladophora albida, and Yuzurua poiteaui var. gemmifera. During the summer rain season, there were three exclusive taxa, Gracilaria flabelliformis subsp. simplex, Halimeda gracilis, and Cl. coelothrix. In the dry season, the exclusive species at this site were Chondria curvilineata, Laurencia caraibica, Halimeda monile, Udotea spinulosa, Cladophoropsis macromeres and C. membranacea (Table 1, Figure 4).
In Villamar, four exclusive taxa were present in the winter rain season, Hypnea spinella, Meristotheca gelidium, Caulerpa ashmeadii, and C. prolifera. In the summer rain season, the exclusive species were Gracilaria caudata J. Agardh, Udotea flabellum, U. unistratea, and Ulva compressa. Finally, in the dry season, there were 19 exclusive species including Padina gymnospora, P. sanctae-crucis, Wurdemannia miniata, Champia parvula var. postrata, and Eucheumatopsis isiformis (Table 1, Figure 4).
In Xpicob, the taxa that were observed in all sampling periods are Acanthophora spicifera, Digenea mexicana, Cladophora crispula, and C. sericea. In Villamar, the taxa that were observed in all sampling periods are Dictyota caribaea, Acanthophora spicifera, Alsidium seaforthii, D. mexicana, Laurencia intricata, Palisada corallopsis, Pterocladiella sanctarum, Hypnea cervicornis, Gracilaria debilis, G. flabelliformis, Halimeda scabra, and Acetabularia crenulata (Table 1, Figure 4).

3.4. Vertical Distribution Profile of Macroalgae

Filamentous algae dominated both in richness and biomass in the intertidal zone at both locations. During the three seasons and in both locations, the fleshy, calcified algae were located at higher depths.
In Xpicob, the highest diversity was observed in the deepest areas (quadrants 4 and 5); this pattern was maintained in winter rains and summer rains and in the dry season; furthermore, quadrant 2 of transect one also presented high diversity (Table 2).
In contrast to Xpicob, Villamar had the highest diversity in the central quadrant (two, three, and four) in winter rains and dry seasons; in summer rain season, the highest diversity was that of quadrant 5 of transect one (Table 2).
In Villamar, we also found fleshy algae with economic importance (such as Meristotheca and Eucheumatopsis) that were not found in Xpicob. At both locations, we found Gracilaria species such as G. cervicornis, G. debilis, or G. flabelliformis; however, in Xpicob, this genus was less represented in terms of the number of species than in Villamar, where G. caudata and G. damicornis were also found.

3.5. Temporal and Spatial Variation of Biomass

In Xpicob, the highest TSB was observed in the winter rain season, and the lowest in the summer rain season (Figure 5, Table 1). In Villamar, the highest TSB was observed in the summer rain season, while the lowest was observed in the dry season (Figure 5, Table 1).
In the winter rain season, the highest biomass value was found in Xpicob; however, in the summer rain and dry seasons, the highest biomass value was found in Villamar. These results were corroborated by a two-way ANOVA, which showed that biomass varied significantly between seasons (F = 0.02429, p = 0.8805) (Figure 5).
The grouping analysis (Cluster) revealed the existence of three groups. Group I was the most dissimilar, constituted only by the summer rain season from Xpicob (9% similarity). Group II was composed of the dry and winter rain seasons of Xpicob (38% similarity). Group III was formed by the three climatic seasons of Villamar (41% similarity) (Figure 6).
Therefore, in terms of biomass, both locations are different from each other, since the cluster analysis showed a group of macroalgae from Villamar and two other separate groups for Xpicob (Figure 6).

3.6. Importance Value Index

3.6.1. Xpicob’s Macroalgae Importance Value Index

During the winter rain season, the species with the highest importance values were: Jania capillacea (IVI = 0.4036), Digenea mexicana (IVI = 0.2328), Halimeda opuntia (IVI = 0.2099), Jania pedunculata var. adhaerens (IVI = 0.1664), Laurencia intricata (IVI = 0.1070), and Alsidium seaforthii (IVI = 0.1051). In the summer rain season, the taxa with the highest importance values were: Cladophora flexuosa (IVI = 0.3435), D. mexicana (IVI = 0.2280), A. seaforthii (IVI = 0.1730), Gracilaria debilis (IVI = 0.1372), Cladophora crispula (IVI = 0.1184), and Laurencia intricata (IVI = 0.1004). Finally, in the dry season, the taxa with the highest importance value were H. opuntia (IVI = 0.4935), J. capillacea (IVI = 0.2454), and Cl. crispula (IVI = 0.09294) (Figure 7).

3.6.2. Villamar’s Macroalgae Importance Value Index

In the winter rain season, the species with the highest importance values were: Gracilaria debilis (IVI = 0.4947), Halimeda incrassata (IVI = 0.2773), Udotea dixonii (IVI = 0.1726), Palisada perforata (IVI = 0.1548), Yuzurua poiteaui (IVI = 0.1047), and Gracilaria cervicornis (IVI = 0.0939). In the summer rain season, the species with the highest importance values were: Cladophora sericea (IVI = 0.2860), Ceramium corniculatum (IVI = 0.2361), Halimeda scabra (IVI = 0.1638), Cladophora laetevirens (IVI = 0.1601), Digenea mexicana (IVI = 0.1568), and Udotea dixonii (IVI = 0.1325). In the dry season, the species with the highest importance value were H. incrassata (IVI = 0.2094), Eucheumatopsis isiformis (IVI = 0.1874), Jania capillacea (0.1476), G. debilis (0.1474), and D. mexicana (0.0940) (Figure 7).

3.7. Macroalgal Community Attributes

3.7.1. Macroalgal Community Attributes

Xpicob

The highest diversity was observed in the winter rain season (H′ = 2.191), followed by the summer rain season (H′ = 2.084), and, finally, the dry season (H′ = 1.492). Because it is directly related to diversity, evenness followed the same pattern, with the lowest evenness value in the dry season (J′ = 0.51) and the highest in the summer rain season (J′ = 0.73). Conversely, dominance is indirectly related to diversity and evenness, so the highest dominance was observed in the dry season; in the two seasons with higher diversity, the dominance presented lower values than in the dry season (Figure 8).

Villamar

During the study period, the alpha diversity increased with time in Villamar; the lowest diversity was observed in the winter rain season (H′ = 1.866) and the highest in the dry season (H′ = 2.823). Evenness, being directly related to diversity, showed a similar pattern. The lowest evenness value was observed in the winter rain season (J′ = 0.587) and the highest in the dry season (J′ = 0.737). The lowest dominance was observed in the dry season (D = 0.0903) and the highest in the winter rain season (D = 0.24) (Figure 9).

3.7.2. β (Beta) Diversity

Xpicob

The turnover of species between the three sampling periods was over 50%; however, the rate of turnover was very similar between the winter rain season and the summer rain season, and between the dry season and the winter rain season (0.5); however, the highest turnover corresponded to the change from the summer rain season to the dry season (0.65) (Table 3).

Villamar

In this location, the species turnover was below 50% and was similar in the three climatic seasons (0.42, 0.46, and 0.48). The highest turnover rate was observed from the dry season to the winter rain season (Table 3).

3.8. Relationship between Environmental Factors and the Species Biomass

The PERMANOVA analysis showed that the environmental variables were significantly different both between locations and seasons (Table 4).
The Analysis of Variance applied to each variable showed that the environmental variables that are significantly different between locations are: salinity (F = 8.3230 p = 0), higher in Xpicob (35.5–39 ppm); depth (F = 27.15 p = 2.21−06), higher in Villamar (240 cm); transparency (F = 55.08 p = 4.36−10); dissolved oxygen (F = 6.8031 p = 0), for which the highest value was observed in Villamar (8–13 mg/L); and the type of substrate, with the rocky substrate prevailing in Villamar (F = 31.22 p = 5.69−7) and the sandy substrate in Xpicob (F = 31.22 p = 5.69−7) (Figure 10).
Comparatively, when analyzing the environmental variables between seasons for each location, the following was observed:
In Xpicob, the environmental variables that were significantly different between seasons were as follows: salinity (F = 1.5330 p = 0), with the lowest salinity value observed in the summer rain season (36 ppm), while in the winter rain and dry seasons, the values were very similar (39.9 and 40 ppm); temperature (F = 51.96 p = 4.67−14), with the highest value observed in the summer rain season (36 °C) and the lowest in the dry season (28 °C); depth (F = 15.22 p = 4.04−06), with the lowest value observed in the summer rain season and the highest in the dry season; transparency (F = 17.04 p = 1.33−06), with the lowest value observed in the summer rain season and the highest in the dry season; and dissolved oxygen (F = 2.1833 p = 0), with the lowest value observed in the summer rain season (5.3 mg/L) and the highest in the winter rain season (13 mg/L) (Figure 10).
In Villamar, the environmental variables that were significantly different between seasons were as follows: salinity (F = 1.5330 p = 0), with the lowest value observed in the winter rain season (34.4 ppm) and the highest in the dry season (36 ppm); temperature (F = 51.96 p = 4.67−14), with the highest value (36 °C) observed in the summer rain season and the lowest in the winter rain season (29 °C); depth (F = 15.22 p = 4.04−06), with the lowest value observed in the summer rain season and the highest in the winter rain season; transparency (F = 17.04 p = 1.33−06), with the lowest value observed in the summer rain season and the highest in the winter rain season; and dissolved oxygen (F = 2.1833 p = 0), with the lowest value in the summer rain season (8 mg/L) and the highest in the winter rain season (13 mg/L) (Figure 10).
In the Canonical Correspondences analysis performed, the first three components explained 69.314% of the total variance. The first component is influenced directly by depth and indirectly by temperature. The second component is directly related to the type of sandy substrate and indirectly related to salinity (Table 5 and Table 6).
There were differences in the composition and biomass of the taxa in both locations in terms of depth. At higher depths and lower temperatures, we found specimens of Meristotheca gelidium, Gracilaria flabelliformis, G. cervicornis, G. debilis, Halimeda opuntia, H. incrassata, H. monile, H. scabra, Udotea spinulosa, U. looensis, U. caribaea, U. dixonii, Caulerpa ashmeadii, and C. prolifera, but also articulated corallines such as Jania capillacea and Amphiroa fragilissima or fleshy thalli of the genus Laurencia. On the other hand, in shallower areas and at higher temperatures, we found filamentous taxa such as Ceramium corniculatum, Cladophora, Lophosiphonia, and Polysiphonia, and blade taxa such as Ulva.
Axis two of the Canonical Correspondence Analysis revealed that the salinity and the type of substrate (sandy) are the factors that determine the biomass and the presence of the taxa at each location. In Xpicob, where the salinity is higher and the sandy substrate dominates, we mainly found filamentous specimens of the genus Cladophora and articulated coralline algae such as Jania, Amphiroa, and Laurencia. In contrast, in Villamar, where a rocky substrate and lower salinity predominate, we found species of fleshy red algae such as Gracilaria debilis and Meristotheca gelidium, calcified green algae of the genera Halimeda, Udotea, and Penicillus, and a few filamentous algae such as Willeella and Cladophora.
Furthermore, the separation of the summer rains season in Xpicob (XL) from its other two seasons was observed again. Similarly, summer rains season in Xpicob (XL) is ordered along the seasons in Villamar (Figure 11).

4. Discussion

4.1. Species Composition

In this study, we performed an ecological analysis of the phycoflora at two locations and identified a total of 74 taxa. These results are different from the report by Ortiz-Rosales (1988) [7], who cited 42 species for three locations in Campeche. This difference could be attributed to the sampling effort, the updated literature, and the meticulous laboratory work for the determination of the taxa.
On the coast of Campeche, there is a total of 271 known algae taxa [4,5,6], only 27% of which were identified in this study; this indicates that floristic studies mainly provide data on the species richness of the place, while ecological studies help understand the distribution patterns of the species in response to environmental conditions [7].
The highest species richness was observed in the class Florideophyceae (Rhodophyta), which is in keeping with previous studies in the area [3,4,5,6] reporting that the Phylum Rhodophyta and the class Florideophyceae are the best represented, in terms of the number of taxa. The success of this group of algae is attributed to their life cycle and reproduction strategies (formation and dispersal of spores) that allow them to persist at different times of the year [37,47].

4.2. Biogeographic Affinity

Lüning (1990) [48] suggests that the location of Campeche near the northern limit of the tropical Atlantic region would explain the high value of the Cheney index observed in this study (23.6), suggesting that the flora of Campeche is typically tropical. The flora of the study site included Acanthophora spicifera, Udotea caribaea, U. cyathiformis, Halimeda incrassata, Gracilaria debilis, Hypnea cervicornis, Chondria floridana, Amphiroa fragilissima, and Laurencia intricata, which are species with a tropical distribution.
The estuaries and coastal flora of the state present Cheney indices between 6.5 and 13 (tropical flora) [5,36]. In our study, we observed high index values, which are attributed to the low richness of brown algae species, with Dictyotales being the only species present. This group of brown algae is considered cosmopolitan since it can be found in both temperate and tropical zones. Furthermore, it has been observed that Dictyotales thalli remain as small branches during adverse periods [49]. In this sense, the sampling method is of great importance since direct sampling was used to evaluate subtidal populations [18]; this is a selective sampling method and, consequently, cannot ensure that all species present at the site are represented in the collection [13]. In the state of Campeche, 27 species of brown algae have been cited [5,6,50]; the Ectocarpaceae family of brown algae is composed entirely of algae of microscopic size that are mostly epiphytes [51]. This observation confirms that the type of sampling and analysis of the specimens greatly influenced the number of brown algae present in this study. In addition, environmental factors such as transparency (suspended organic matter), temperature, and depth influence the presence of brown algae. Reportedly, brown algae have their highest diversity in cold water environments such as the Pacific coastal zone of Baja California, which is influenced by the California Current (cold water) and upwelling that provide cold water that is rich in nutrients [37,52].

4.3. Spatial and Temporal Variation of Species Richness

In this work, the highest richness was observed in the dry season and the lowest in the winter rain season. This same variation in richness was observed by Mateo-Cid et al. (2013) [5] for eight locations on the coast of Campeche; Alfonso and Martinez-Daranas (2009) [53] reported a similar pattern for the northeast of Cuba. Increased richness in dry seasons and low richness in summer rains season can be attributed to the high transparency (illumination) typical of the dry months.
The classes Florideophyceae and Ulvophyceae had a different species richness at each sampling time, with Florideophyceae being the most diverse in the winter rain and dry seasons. Ulvophyceae, on the other hand, had the highest richness in the summer rain season, which can be attributed both to the intrinsic characteristics of the representatives of each Phylum at the time of sampling. Brown and green algae are annual, while red algae are both annual and perennial [54].
The taxa that were present during the three sampling periods were mainly perennial algae such as Digenea mexicana, Acanthophora spicifera, and Gracilaria debilis, which are characterized by a life cycle lasting more than one year. Annual algae such as Cladophora, Polysiphonia, Lophosiphonia, or Ceramium were also recorded throughout the three sampling periods, with life cycles that last less than a year with several generations [5,55].

4.4. Vertical Distribution Profile of Macroalgae

At both sampling locations at low depths (50–70 cm, the most exposed area), we found filamentous algae forming aggregates, mainly from the class Ulvophyceae, which are considered opportunistic [56]. In keeping with this observation, Lubchenco and Menge (1978) [57] indicated that the presence, and biomass, of filamentous and lamellar algae increase in areas of higher exposure to waves, limiting the establishment of other types of fleshy or calcareous algae. This result coincides with our observations in the first quadrants of the transects, where mainly Ulvophyceae and Florideophyceae filamentous algae were found; in addition to being opportunistic, these organisms (e.g., Ceramium corniculatum, Polysiphonia subtilissima, Cladophora albida, and C. coelothrix) have rapid growth rates.
Various authors [58,59] have studied the colonization and succession process of seaweeds, reporting that the colonization is initially composed of pioneer organisms with short life cycles and high reproduction rates, which modify the characteristics of the substrate. Delgado et al. (2008) [60], report that in the coastal splashing zone, there is a horizontal distribution of algae, and that the community is homogeneous and has a lower number of species, which is in keeping with what we observed in the present study: the shallow areas that are more exposed to waves have a lower diversity of algae. Furthermore, due to the sunlight available in the area, filamentous algae can grow rapidly with high photosynthetic rates per unit of biomass and rapid O2 production rates [59].
Mathieson (1989) [61] reported a higher stability in deeper communities composed mainly of perennial algae; however, the richness was lower compared to that of shallower communities. Coleman and Mathieson (1975) [62] hypothesized that, in shallow waters with wide temperature fluctuations, the number of annual algae would be higher than that of perennial algae. This may explain the dominance of annual filamentous algae in the shallow waters that predominated in Xpicob and Villamar.

4.5. Temporal and Spatial Variation of the Biomass

In our study, the variation in total annual biomass was very marked; the annual biomass value recorded in the winter rain season in Xpicob was 10 times higher (322.24 g) than that of the summer rain season (23.43 g); this is possibly due to transparency, which is an environmental factor that varied throughout the seasons in Xpicob. At this site, the highest incidence of light was observed, which causes species of tropical affinity to reach their maximum biomass. These results coincide with what was recorded by Li-Alfaro and Zafra-Téllez (2012) [63] for the macroalgae community of Puerto Malabrigo, Peru.
In contrast, in Villamar, the biomass did not vary throughout the sampling cycle, having values between 200 g/m2 and 250 g/m2. These biomass values were higher than those observed in a similar study in Campeche [7] where the highest dry biomass value was 225 g/m2.
Ortiz-Rosales (1998) [7] pointed out that Eucheumatopsis isiformis and Acanthophora spicifera were the most important species in terms of biomass (20–40%) (Champotón, Isla Arena and Sabancuy), mainly because these taxa are in deep areas (150–250 cm) with high transparency, which allows the photosynthetic rate to be higher and increases biomass.
Quirós-Rodríguez et al. (2010) [64] reported that filamentous algae present biomass values below 1, which coincides with our observation that the highest biomass values were given by leathery and fleshy species.
It should be noted that in most studies of marine macroalgae, the calculation of biomass is estimated from the cover (visually using photography). Few studies use biomass as an indicator of abundance, including those of Martinez-Daranas et al. (2016) [19] and Zúñiga-Ríos et al. (2012) [65]. The estimation of macroalgae biomass is of interest to many disciplines, and is useful in different ways, for example, it is a measure of the resource available for organisms at other trophic levels; furthermore, it provides information on the profitability of their exploitation as a natural resource [63]. Furthermore, the amount of biomass of macroalgae is related to factors such as light, temperature, nutrients, and type of substrate [19].
The clustering analysis showed the formation of three groups. Group I was formed only by Xpicob in the summer rain season; we thus infer that in this season, the number of taxa shared with the other seasons is low (four), compared to the dry and winter rain seasons with seven shared species. Furthermore, in Xpicob, the biomass values of the summer rain season were below 3 g/m2, while in the dry and winter rain seasons, the biomass values were between 0.01 g/m2 and 100 g/m2.
Additionally, the environmental variables measured in Xpicob in the summer rain season were significantly different from those in the dry and winter rain seasons (which were alike). We thus infer that during the summer rain season, the environment is characterized by very particular environmental conditions. Therefore, low numbers of various species of filamentous algae, or the absence of articulated corallines, such as Jania or Amphiroa, are observed [53].
Group II of the cluster analysis includes the three climatic seasons of Villamar, even if the summer rain season had lower levels of similarity. The three climatic seasons of Villamar shared a total of 12 species. Jania capillacea and Amphiroa fragilissima were only found in the winter rain and dry seasons, but not in the summer rain season.

4.6. Macroalgal Community Attributes

4.6.1. α Diversity

Villamar was the location that presented the highest diversity. Compared to Xpicob, Villamar is deeper, which, combined with the predominance of a rocky substrate with both protected and exposed areas, allows the establishment, development, and growth of macroalgae. It has been reported that higher topographic variations result in a higher floristic diversity [66].
Rocky coasts are generally covered with vegetation formed almost exclusively by macroalgae [67]. Coasts with soft and sandy bottoms, on the other hand, have a lower abundance of macroalgae, mainly because most species are unable to attach to an unstable substrate with continuous water movement [66,67].
The highest α diversity was observed in the winter rain season and the lowest in the dry season, which contrasts with previous studies [7,37] reporting that the highest diversity was observed in the dry season when the temperature reaches the highest value, favoring the increase in species richness. In keeping with this idea, Núñez-López (1996) [68] indicated that the lowest values of richness and biomass of macroalgae are observed in the winter season when the water temperature reaches its lowest value.
Although the range of species richness between the three seasons in Xpicob is 2–8 species, there is a significant difference in the biomass of the species in the winter rain season, since at this time, the biomass was over 300 g, while in the remaining two seasons, the biomass was below 150 g.
Villamar presents an opposite pattern relative to Xpicob; the highest diversity was observed in the dry period, and the lowest in the winter rain season, coinciding with Ortiz-Rosales (1988) [7], possibly because in this season, environmental conditions such as temperature and salinity promote the increase in richness and biomass of macroalgae [69].
The Pielou evenness index presented values close to 1 in the summer rain season for Xpicob and in the dry season for Villamar, which indicates that there are no species with dominant abundance, suggesting that the macroalgae community is homogeneously distributed in these seasons. However, in the dry season of Xpicob and the winter rain season of Villamar, the Pielou evenness index was below 0.6, which, in turn, is related to alpha diversity, since in the same seasons, the diversity was lower at both locations. This observation indicates that the algae community at both sampling locations might be heterogeneously distributed, with one or several dominating species, in terms of abundance. These results coincide with the spatial behavior of macroalgae diversity in Ascensión Bay, reported by Fernández-Prieto (1988) [70].

4.6.2. β Diversity

In Xpicob, the turnover of species between seasons was higher than 0.5, which indicates that at least 50% of the species was replaced in each season. In contrast, in Villamar, the species turnover rate was below 50% in the three sampling periods.
This turnover rate is in turn related to the biological type of each species [55], since annual species that are present for a short period (short life cycle) are replaced by other species in the following season. Perennial algae, on the other hand, have life cycles that last more than one year, allowing them to be present in all seasons, thus reducing their turnover rate. In Villamar, perennial species were predominant, but in Xpicob, annual species were predominant; this could explain why the turnover rate at each location was above or below 50%.

4.7. Relationship between Environmental Factors and the Biomass of Taxa

According to our ACC results, the factors that explain the highest variation in the seasonal or temporal biomass of the taxa are depth, temperature, salinity, and type substrate (mostly sandy substrate). Environmental factors influence and determine the establishment, growth, reproduction, distribution, and abundance of algae in a specific location; similarly, the temporal fluctuations of these factors are related to the seasonal variations of algae [20].
It has been observed that temperature influences the reproduction of algae. In brown algae, for example, low temperatures cause the production of gametes, while high temperatures promote the formation of spores [11].
Salinity not only affects the distribution of algae but also their reproduction, causing the release of spores and polyspermy and influencing the viability of gametes [71].
It is important to emphasize that most environmental factors act together; for example, in tropical areas, changes in light intensity and/or temperature induce the synchronous release of gametes of holocarpic green algae (the entire thallus is transformed into gametes) [72,73].
The ACC showed that the substrate (mostly sandy) has a great influence on the biomass and composition of the macroalgae communities in both locations. Saad-Navarro and Riosmena-Rodríguez (2005) [54] in Baja California Sur, Alfonso and Martínez-Daranas (2009) [53] in Cuba, and Quirós-Rodríguez et al. (2010) [64] in Colombia concluded that climatic seasons do not determine the temporal variation of abundance and composition of algae; rather, the particular conditions and characteristics of each site influence the composition and abundance of macroalgae, mainly due to the type of substrate. McCook et al. (2001) [74] and other authors have shown that the sandy substrate negatively affects the coverage of algal associations; even in sandy bottoms with pebbles, algal richness is higher than in completely sandy or muddy bottoms [75].
Ortiz-Rosales (1988) [7] in Campeche and Delgado et al. (2008) [60] in Colombia reported that the substrate, depth, temperature, transparency, and salinity are the factors that exert the highest influence on the presence, composition, and abundance of macroalgae. It has been widely demonstrated by several reports [7,53,64,76] that the substrate greatly influences the algal composition of a given location; most macroalgae, especially Rhodophyta, adhere mainly to rocky substrates, which gives them a higher stability than sandy substrates. However, there are various macroalgae species (Halimeda, Penicillus, and Udotea, among others) that use rhizoids as a fixation system, which allows them to establish and develop in sandy substrates and they are thus considered substrate-forming organisms [54,76,77].

5. Conclusions

Florideophyceae stood out in terms of specific richness and dominance, with depth being the factor that favored its distribution of red algae, while for Ulvophyceae, the factor that influenced its distribution was the type of substrate. The analyzed communities present low similarity in both composition and abundance, which suggests that they are different communities, and the behavior of their attributes is different in each location. The turnover of species in both locations was high, considering that in each season, the turnover was more than 50%, which indicates that both locations have different environmental conditions in each season, causing the community to vary according.
This study demonstrates that it can be used for conservation and use studies of various species such as the agarophyte Gracilaria debilis.

Author Contributions

Conceptualization, methodology, C.M.H.-C., Á.C.M.-G. and L.E.M.-C.; methodology, C.M.H.-C., Á.C.M.-G., D.Y.G.-L. and L.E.M.-C.; investigation, C.M.H.-C., Á.C.M.-G. and L.E.M.-C.; formal analysis, C.M.H.-C., Á.C.M.-G. and L.E.M.-C.; writing original draft, C.M.H.-C., Á.C.M.-G., D.Y.G.-L. and L.E.M.-C.; data curation, C.M.H.-C., Á.C.M.-G., D.Y.G.-L. and L.E.M.-C.; writing—review and editing, C.M.H.-C., Á.C.M.-G., D.Y.G.-L. and L.E.M.-C.; funding acquisition, L.E.M.-C. and Á.C.M.-G. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Instituto Politécnico Nacional (SIP 20170696, 20180489, 20195092, 20170767, 20180491 y 20195127), for providing financial support, facilities, and necessary equipment for the development of this study.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The raw data supporting the conclusions of this article will be made available by the authors on request.

Acknowledgments

C.M.H.-C. appreciate the scholarship granted by Consejo Nacional de Humanidades Ciencias y Tecnologías (CONAHCyT) (scholarship number 704348). Á.C.M.-G., L.E.M.-C. appreciate the scholarship granted by the Commission for the Operation and Promotion of Academic Activities (COFAA) and the EDI incentives. To A. Gerardo Garduño Acosta, J. Alfredo Pérez Salgado, Itzel Gonzáles Contreras, Ángel Norberto Ocaña Valencia for their logistical support.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Location of the study area (Campeche) and sampling locations (Xpicob and Villamar) (Hernández-Casas C.M.).
Figure 1. Location of the study area (Campeche) and sampling locations (Xpicob and Villamar) (Hernández-Casas C.M.).
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Figure 2. Total richness of macroalgae species in Xpicob and Villamar, Campeche, during the sampling periods performed in the winter rain (October 2016), dry (April 2017), and summer rain seasons (August 2017).
Figure 2. Total richness of macroalgae species in Xpicob and Villamar, Campeche, during the sampling periods performed in the winter rain (October 2016), dry (April 2017), and summer rain seasons (August 2017).
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Figure 3. Seasonal species richness of each class of macroalgae in Villamar and Xpicob, Campeche, during the sampling periods performed in the winter rain (October 2016), dry (April 2017), and summer rain seasons (August 2017).
Figure 3. Seasonal species richness of each class of macroalgae in Villamar and Xpicob, Campeche, during the sampling periods performed in the winter rain (October 2016), dry (April 2017), and summer rain seasons (August 2017).
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Figure 4. Seaweeds that are reported as exclusive for some climatic season in Xpicob and Villamar Campeche during sampling. (A) Padina santae-crucis, (B) Acanthophora spicifera, (C) Meristotheca gelidium, (D) Caulerpa ashmeadii, (E) Halimeda scabra.
Figure 4. Seaweeds that are reported as exclusive for some climatic season in Xpicob and Villamar Campeche during sampling. (A) Padina santae-crucis, (B) Acanthophora spicifera, (C) Meristotheca gelidium, (D) Caulerpa ashmeadii, (E) Halimeda scabra.
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Figure 5. Average biomass (g/m2) and standard error, of X: Xpicob and V: Villamar, Campeche, in each climatic season (N, Winter rain season; L, Summer rain season; and S, Dry season).
Figure 5. Average biomass (g/m2) and standard error, of X: Xpicob and V: Villamar, Campeche, in each climatic season (N, Winter rain season; L, Summer rain season; and S, Dry season).
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Figure 6. UPGMA clustering analysis using Bray–Curtis similarity. XS, Xpicob—dry season; XN, Xpicob—winter rain season; XL, Xpicob—summer rain season; VN, Villamar—winter rain season; VS, Villamar—dry; VL, Villamar—summer rain season.
Figure 6. UPGMA clustering analysis using Bray–Curtis similarity. XS, Xpicob—dry season; XN, Xpicob—winter rain season; XL, Xpicob—summer rain season; VN, Villamar—winter rain season; VS, Villamar—dry; VL, Villamar—summer rain season.
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Figure 7. Seaweeds that are reported as dominants for some climatic season in Xpicob and Villamar Campeche during sampling. (A) Digenea mexicana, (B) Eucheumatopsis isiformis, (C) Gracilaria debilis, (D) Palisada perforata and Yuzurua poiteaui, (E) Halimeda incrassata.
Figure 7. Seaweeds that are reported as dominants for some climatic season in Xpicob and Villamar Campeche during sampling. (A) Digenea mexicana, (B) Eucheumatopsis isiformis, (C) Gracilaria debilis, (D) Palisada perforata and Yuzurua poiteaui, (E) Halimeda incrassata.
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Figure 8. Estimation of alpha diversity (Shannon–Wiener), evenness, and dominance in Xpicob for the three climatic seasons.
Figure 8. Estimation of alpha diversity (Shannon–Wiener), evenness, and dominance in Xpicob for the three climatic seasons.
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Figure 9. Estimation of alpha diversity (Shannon–Wiener), evenness, and dominance in Villamar for the three climatic seasons.
Figure 9. Estimation of alpha diversity (Shannon–Wiener), evenness, and dominance in Villamar for the three climatic seasons.
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Figure 10. ANOVA of the environmental variables measured in Xpicob (black line) and Villamar (red line), Campeche, in October (2016), April (2017), and August (2017). (A) ANOVA of salinity, (B) ANOVA of temperature, (C) ANOVA of Depth, (D) ANOVA of Transparency, (E) ANOVA of rocky substrate, (F) ANOVA of sandy substrate, and (G) ANOVA of dissolved oxygen.
Figure 10. ANOVA of the environmental variables measured in Xpicob (black line) and Villamar (red line), Campeche, in October (2016), April (2017), and August (2017). (A) ANOVA of salinity, (B) ANOVA of temperature, (C) ANOVA of Depth, (D) ANOVA of Transparency, (E) ANOVA of rocky substrate, (F) ANOVA of sandy substrate, and (G) ANOVA of dissolved oxygen.
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Figure 11. Canonical correspondence analysis (ACC) for environmental variables and biomass of macroalgae species by quadrant and season in Xpicob and Villamar, Campeche, collected in 2016 and 2017. Sites (quadrants) of Xpicob (purple circle). Sites (quadrants) of Villamar (pink circle). Macroalgae species located in shallow areas (green circle). Species of macroalgae located in deep areas (blue circle).
Figure 11. Canonical correspondence analysis (ACC) for environmental variables and biomass of macroalgae species by quadrant and season in Xpicob and Villamar, Campeche, collected in 2016 and 2017. Sites (quadrants) of Xpicob (purple circle). Sites (quadrants) of Villamar (pink circle). Macroalgae species located in shallow areas (green circle). Species of macroalgae located in deep areas (blue circle).
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Table 1. List of taxa located in Xpicob and Villamar, Campeche, during the three seasons (winter rain season, dry season, and summer rain season) during the sampling period (2016–2017). Also, its show the specific temporality biomass in a heat map where, deep red: lower values and deep blue: higher values.
Table 1. List of taxa located in Xpicob and Villamar, Campeche, during the three seasons (winter rain season, dry season, and summer rain season) during the sampling period (2016–2017). Also, its show the specific temporality biomass in a heat map where, deep red: lower values and deep blue: higher values.
VillamarXpicob
SpeciesWinter RainsSummer RainsDryWinter RainsSummer RainsDry
Phylum Heterokontophyta
Class Phaeophyceae
   Order Dictyotales
      Family Dictyotaceae
1Dictyota caribaea Hörnig & Schnetter0.781.550.07 0.01
2Padina gymnospora (Kützing) Sonder 0.56
3Padina sanctae-crucis Børgesen 0.01
Phylum Rhodophyta
Class Florideophyceae
   Order Corallinales
      Family Corallinaceae
4Jania capillacea Harvey 0.6649.03
5Jania pedunculata var. adhaerens (J. V. Lamouroux) A. S. Harvey, Woelkerling & Reviers0.7716.69 107.0731.2
      Family Lithophyllaceae
6Amphiroa fragilissima (Linnaeus) J. V. Lamouroux0.01 2.813.99
   Order Ceramiales
      Family Ceramiaceae
7Ceramium corniculatum Montagne 54.252.50.46 1.56
      Family Rhodomelaceae
8Acanthophora spicifera (M. Vahl) Børgesen4.613.271.698.970.260.97
9Alsidium seaforthii (Turner) J. Agardh2.221.747.9810.862.38
10Alsidium triquetrum (S. G. Gmelin) Trevisan 0.330.2 0.62
11Chondria curvilineata Collins & Hervey 0.01
12Chondria floridana (Collins) M. Howe 1.571.03
13Chondria leptacremon (Melvill ex G. Murray) De Toni 1.3
14Digenea mexicana G. H. Boo & D. Robledo1.5715.186.3642.834.1
15Laurencia caraibica P. C. Silva 0.16
16Laurencia filiformis (C. Agardh) Montagne0.170.820.92.280.01
17Laurencia intricata J. V. Lamouroux 2.36 0.02
18Laurencia obtusa (Hudson) J. V. Lamouroux 3.21
19Laurencia viridis Gil-Rodríguez & Haroun 4.37
20Lophosiphonia obscura (C. Agardh) Falkenberg 0.010.01
21Palisada corallopsis (Montagne) Sentíes, Fujii & Díaz-Larrea4.510.791.182.34 0.1
22Palisada perforata (Bory) K. W. Nam23.06 8.240.86 4.22
23Polysiphonia subtilissima Montagne 4.44 0.08
24Yuzurua poiteaui (J. V. Lamouroux) Martin-Lescanne8.8 4.4314.1
25Yuzurua poiteaui var. gemmifera (Harvey) M. J. Wynne 0.84
      Family Pterocladiaceae
26Pterocladiella sanctarum (Feldmann & Hamel) Santelices0.010.641.140.80.52
   Order Gigartinales
      Family Cystocloniaceae
27Hypnea cervicornis J. Agardh0.330.040.01 0.84
28Hypnea spinella (C. Agardh) Kützing0.28
      Family Solieriaceae
29Eucheumatopsis isiformis (C. Agardh) Núñez-Reséndiz, Dreckmann & Sentíes 29.04
30Meristotheca gelidium (J. Agardh) E. J. Faye & M. Masuda0.38
31Wurdemannia miniata (Sprengel) Feldmann & Hamel 0.68
   Order Gracilariales
      Family Gracilariaceae
32Gracilaria caudata J. Agardh 1.15
33Gracilaria cervicornis (Turner) J. Agardh6.620.26 6.7
34Gracilaria damicornis J. Agardh 1.58
35Gracilaria debilis (Forsskål) Børgesen83.515.3526.050.862.88
36Gracilaria flabelliformis (P. Crouan & H. Crouan) Fredericq & Gurgel0.50.10.080.83 0.06
37Gracilaria flabelliformis subsp. simplex Gurgel, Fredericq & J. N. Norris 0.32
   Order Halymeniales
      Family Halymeniaceae
38Codiophyllum mexicanum Núñez-Resendiz, Dreckmann & Sentíes 2.04
   Order Rhodymeniales 0.02
      Family Champiaceae
39Champia parvula var. prostrata L. G. Williams
Phylum Chlorophyta
Class Ulvophyceae
   Order Bryopsidales4.07
      Family Caulerpaceae 0.030.045
40Caulerpa ashmeadii Harvey0.09
41Caulerpa fastigiata Montagne
42Caulerpa prolifera (Forsskål) J. V. Lamouroux 0.32
      Family Halimedaceae 0.82
43Halimeda discoidea Decaisne43.6920.7233.296.850.14
44Halimeda gracilis Harvey ex J. Agardh 1.71 4.17
45Halimeda incrassata (J. Ellis) J. V. Lamouroux 0.68 44.64 68.79
46Halimeda monile (J. Ellis & Solander) J. V. Lamouroux1.316.943.33
47Halimeda opuntia (Linnaeus) J. V. Lamouroux 2.40.51
48Halimeda scabra M. Howe 0.010.01
49Halimeda tuna (J. Ellis & Solander) J. V. Lamouroux4.510.791.182.34 0.1
50Penicillus capitatus Lamarck 0.150.03
51Udotea caribaea D. S. Littler & Littler 7.46
52Udotea conglutinata (J. Ellis & Solander) J. V. Lamouroux 5.97
53Udotea cyathiformis Decaisne 1.92
54Udotea cyathiformis var. flabellifolia D. S. Littler & Littler 6.65
55Udotea dixonii D. S. Littler & Littler14.289.11 3.95
56Udotea dotyi D. S. Littler & Littler 1.96
57Udotea flabellum (J. Ellis & Solander) M. Howe 2.63
58Udotea looensis D. S. Littler & Littler0.60.20.04 0.16
59Udotea luna D. S. Littler & Littler 0.3
60Udotea spinulosa M. Howe 0.25
61Udotea unistratea D. S. Littler & Littler 0.72
   Order Cladophorales
      Family Boodleaceae
62Cladophoropsis macromeres W. R. Taylor 2.02
63Cladophoropsis membranacea (Hofman Bang ex C. Agardh) Børgesen 2.04 10.61
      Family Cladophoraceae
64Cladophora albida (Nees) Kützing 1.14
65Cladophora coelothrix Kützing 0.01
66Cladophora crispula Vickers 0.941.7711.33
67Cladophora flexuosa (O. F. Müller) Kützing 5.75 8.051.81
68Cladophora laetevirens (Dillwyn) Kützing 35.250.020.541.85
69Cladophora sericea (Hudson) Kützing 66.73 4.610.750.91
70Willeella brachyclados (Montagne) M. J. Wynne 2.110.670.02
   Order Dasycladales
      Family Polyphysaceae
71Acetabularia crenulata J. V. Lamouroux0.010.010.06
72Acetabularia farlowii Solms-Laubach 0.01
   Order Ulvales
      Family Ulvaceae
73Ulva compressa Linnaeus 0.02
74Ulva flexuosa Wulfen 0.13
Table 2. Variation of Shannon–Wiener diversity for Xpicob and Villamar, in the three climatic seasons at the different depths sampled (quadrants).
Table 2. Variation of Shannon–Wiener diversity for Xpicob and Villamar, in the three climatic seasons at the different depths sampled (quadrants).
XpicobVillamar
Winter RainsSummer RainsDryWinter RainsSummer RainsDry
T1C11.04 0.024
T1C21.0281.0370.9741.0990.4721.969
T1C30.9360.9460.7530.6660.5381.503
T1C41.251 0.6930.4881.1450.896
T1C51.1661.2281.0410.3651.807
T2C11.0630.951 0.81600.494
T2C21.3011.017 0.709 1.103
Table 3. Beta diversity (species turnover) of macroalgae species between climatic seasons for Xpicob and Villamar.
Table 3. Beta diversity (species turnover) of macroalgae species between climatic seasons for Xpicob and Villamar.
LocalitiesSeasonsβ Diversity
XpicobWinter rains–Summer rains0.5
Summer rains–Dry0.6571
Dry–Winter rains0.5111
VillamarWinter rains–Summer rains0.4285
Summer rains–Dry0.4615
Dry–Winter rains0.4857
Table 4. Two-way PERMANOVA analysis for the environmental variables in each location.
Table 4. Two-way PERMANOVA analysis for the environmental variables in each location.
Sum of SquaresdfMean SquaresFp
Locality0.829610.829619.41601
Season1.030220.5150912.05501
Interaction0.05003920.0250190.585550.0653
Residual2.6919630.042728
Total4.601768
Table 5. Correlation coefficient between the environmental variables recorded in Xpicob and Villamar, Campeche (2016–2017) and the biomass (in grams) of the macroalgae observed at both locations.
Table 5. Correlation coefficient between the environmental variables recorded in Xpicob and Villamar, Campeche (2016–2017) and the biomass (in grams) of the macroalgae observed at both locations.
Environmental VariableAxi 1Axi 2Axi 3Axi 4Axi 5Axi 6
Salinity6−0.9820.1160.030−0.0610.135
Temperature−0.222−0.385−0.145−0.203−0.507−0.695
Depth0.9580.0800.1870.0930.1080.146
Transparency0.914−0.0500.1810.0960.3350.089
dissolved oxygen0.3750.4190.269−0.5710.4660.263
Rocky substrate0.1850.618−0.7280.076−0.216−0.029
Sandy Substrate−0.185−0.6180.728−0.0760.2160.029
Table 6. Percentage of variance explained in each axis of the Canonical Correspondence Analysis.
Table 6. Percentage of variance explained in each axis of the Canonical Correspondence Analysis.
EigenvalueVariance (%)Accumulate Variance (%)
Axi 10.78035.44935.449
Axi 20.42119.14654.594
Axi 30.32414.72069.314
Axi 40.25211.44080.754
Axi 50.2149.72490.479
Axi 60.2109.521100
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Hernández-Casas, C.M.; Mendoza-González, Á.C.; García-López, D.Y.; Mateo-Cid, L.E. Spatio-Temporal Structure of Two Seaweeds Communities in Campeche, Mexico. Diversity 2024, 16, 344. https://doi.org/10.3390/d16060344

AMA Style

Hernández-Casas CM, Mendoza-González ÁC, García-López DY, Mateo-Cid LE. Spatio-Temporal Structure of Two Seaweeds Communities in Campeche, Mexico. Diversity. 2024; 16(6):344. https://doi.org/10.3390/d16060344

Chicago/Turabian Style

Hernández-Casas, Cynthia Mariana, Ángela Catalina Mendoza-González, Deisy Yazmín García-López, and Luz Elena Mateo-Cid. 2024. "Spatio-Temporal Structure of Two Seaweeds Communities in Campeche, Mexico" Diversity 16, no. 6: 344. https://doi.org/10.3390/d16060344

APA Style

Hernández-Casas, C. M., Mendoza-González, Á. C., García-López, D. Y., & Mateo-Cid, L. E. (2024). Spatio-Temporal Structure of Two Seaweeds Communities in Campeche, Mexico. Diversity, 16(6), 344. https://doi.org/10.3390/d16060344

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