Phytoplankton Structure in a Coastal Region of the Eastern Entrance of the Gulf of California during La Niña 2022

Abstract

This paper assessed the phytoplankton structure and its relationship with the physical environment in the coastal region off Mazatlán, Mexico, in two seasons of 2022, a year in which a strong La Niña event took place: (1) the warmer (August) and (2) the transitional period to the cold phase (November), based on hydrographic data and samples collected in two systematic scientific expeditions. The results showed clear differences between both seasons. Regarding total abundance, August reached 125,200 cells L⁻¹, while November amounted to 219,900 cells L⁻¹. Regarding species composition, the diatoms Cylindrotheca closterium and Planktoniella sol were dominant in August, while Thalassionema nitzschioides and Tetramphora decussata dominated the assemblages in November. The dinoflagellate Protoperidinium punctulatum was dominant in both seasons. However, very marked differences in its abundance are reported. The differences observed in the species richness and abundance could be attributed to the physical configuration of the water column, particularly the surface temperature, which showed clear changes between both seasons. The results presented here confirmed the high phytoplankton richness (some of them with the potential to generate harmful algal blooms), abundance, and diversity values of the region, suggesting a strong relationship with the physical environment.

1. Introduction

The El Niño Southern Oscillation (ENSO) is one of the main oceanic–atmospheric phenomena that generate high variability in the Earth’s climate system, affecting the biological productivity of both oceanic and coastal environments [1]. Characterized by a warm/cold phase (El Niño/La Niña), ENSO events have been associated with the advection of warm and oligotrophic water masses that decrease species richness and biological productivity during El Niño, while an inverse pattern (increases in both parameters) has been reported due to the presence of cold-water masses enriched with nutrients during La Niña [2].

The Mazatlán coastal region (hereafter MCR) is located at the eastern entrance of the Gulf of California (GoC) (Figure 1), which is recognized as one of the most diverse marine ecosystems and for being one of the 64 large marine ecosystems (LMEs) of the world [3,4]. As part of an LME, the MCR is also recognized for its high productivity levels and as a habitat for the refuge, feeding, and growth of numerous emblematic species, some threatened [5]. The region is recognized for supporting numerous endemic species and being migratory birds’ resting and nesting habitat [6]. The high levels of biological production that the MCR supports are directly related to the organisms located at the base of the pelagic trophic chain, such as phytoplankton.

Phytoplankton comprises a large and heterogeneous group of mainly photosynthetic organisms that provide numerous services to the ecosystem, including the release of oxygen and the sequestration of CO₂ through the process of photosynthesis that they perform, which contributes to the biological or carbon pump [7]. Additionally, being organisms positioned at the base of the trophic chain, they support the production of numerous species with both ecological and economic value, which benefits different fisheries of high commercial value [8]. Recently, phytoplankton have been named “sentinel” organisms of climate change due to their capacity to respond quickly to multiple stressors [9].

Studies of the phytoplankton communities in the MCR began in the 1980s. Pioneering studies revealed a high species richness with high abundance. For example, one of the first taxonomic listings documented 73 species during winter [10], 76 species in spring [11], 67 species in summer [12] and 69 species during autumn [13]. In all cases, diatoms were the dominant organisms, constituting more than 60% of the total abundance.

Some authors, a few years later, confirmed the predominance of diatoms in the region. Indeed, Cortes-Altamirano et al. [14] reported 22 diatom species as the most diverse group in the MCR. Alonso-Rodríguez et al. [15] analyzed the relative abundance of the phytoplankton groups in the outflow of the Urias coastal lagoon into the MCR. They noted that the diatoms were the best-represented group with an abundance of 70%.

Due to these first taxonomic studies, it was also possible to identify many species that generate harmful algal blooms. One of the first reports of harmful algal blooms in the MCR was published by Cortés-Altamirano [16] who documented algal blooms originated by the dinoflagellates Gymnodinium catenatum H.W. Graham 1943 and Ceratium tripos f. ponticum Schiller 1937 [now called Tripos muelleri f. ponticus] by the ciliate Mesodinium rubrum Lohmann 1908 and by the diatom Skeletonema costatum Cleve 1873; these blooms were associated with a high mortality of fish, crustaceans and annelids. Later, Cortes-Altamirano et al. [17] documented the proliferation of the dinoflagellate Prorocentrum triestinum J. Schiller 1918 that reached values of 31,584 cells L⁻¹ without observing any manifestation of toxicity or mortality of fishes. A description of the species of the genus Prorocentrum in the MCR was published by Hernández-Becerril et al. [18], who identified three additional species of the genus that generated algal blooms, P. dentatum Stein 1883, P. minimum J. Schiller 1933 [now called as P. cordatum J.D. Dodge 1976] and P. mexicanum Osorio-Tafall 1942. In addition to these studies, it has been identified that the MCR supports a high density of nitrogen-fixing phytoplankton species, such as Trichodesmium erythraeum Ehrenberg ex Gomont 1892, whose abundances can exceed 60 × 10⁴ cells L⁻¹ [19].

Previous investigations have identified that the MCR supports a high phytoplankton richness (some potentially generating harmful algal blooms) with high abundance. However, these studies have focused on describing the species and providing taxonomic lists without considering the role played by the physical environment in the species composition and in particular the role that ENSO events play. In addition, the studies have been fragmented and use nomenclature that has constantly changed during the last few decades.

As a consequence of the above scenario, this study aimed to assess the phytoplankton structure in the MCR, analyzing the role exerted by the physical environment in two seasons during the La Niña 2022 event, the warm and transitional period to the cold phase. To achieve this, two multidisciplinary scientific expeditions were carried out in August and November of 2022 to collect water samples for phytoplankton cell determinations and acquire high-resolution hydrographic data. We aim to contribute to the knowledge of the phytoplankton population dynamics of the region and determine how it responds to environmental changes. In this sense, it is important to note that a long La Niña event characterized the oceanographic conditions in the Pacific Ocean and surrounding environments during 2022. For example, based on the Multivariate ENSO Index version 2 (MEI v2) [20], during August, the numerical value of this index was −1.8, while in November, it was −1.5, which means that a strong La Niña event took place during each sampling expedition; the last represents a window of opportunity to analyze the role of this event on the structure of the phytoplankton community of the region. Furthermore, with this study, we intend to update the taxonomic list of the phytoplankton species present in the MCR in two contrasting seasons.

In a climate change context, studies that evaluate ecological aspects of the phytoplankton communities become imperative. Particularly for the MCR, in recent years, a trend toward an increase in the sea surface temperature levels has been noted [21] with an upward trend in the frequency and toxicity of harmful algal bloom events [22]. Therefore, studies that analyze the taxonomic composition of phytoplankton and its relationship with the physical environment in different climatic seasons are necessary to establish baseline studies and thus have comparison criteria to identify and understand the threats to which the MCR is subject. With the above, updating and improving strategies for conserving the region’s resources would be possible.

2. Materials and Methods

2.1. Study Area

The MCR is located in the Mexican Pacific, off the coastal state of Sinaloa, Mexico, in the connection between the Pacific Ocean and the GoC (Figure 1A). The region is surrounded by two main islands (Pajaros and Venados), which are considered by the Mexican authorities to be protected areas because they host many species (Figure 1B).

As part of the LME of the GoC, the MCR agrees, in general terms, with the oceanic and atmospheric circulation pattern of the gulf. A tropical–subtropical climate dominates with two distinctive and contrasting phases: the wet from July to October and the dry from November to June when rainfalls are extremely low [23]. The wind circulation pattern is influenced by the seasonal migration of the Intertropical Convergence Zone and by the incidence of the atmospheric pressure centers that present rearrangements in their position according to each season, resulting in a monsoon climate with winds that present an inverse pattern depending on the time of year. During the summer, weak and wet southeasterly winds (5 m·s⁻¹) predominate, while in winter and spring, strong, cold, and dry northwesterly winds (>12 m·s⁻¹) are present [24]. This wind pattern is one of the main mechanisms that generate coastal upwelling in the region, which determines the rates of primary production [23].

In hydrographic terms, three main water masses have been reported in the region: (1) the California Current Water, (2) the Gulf of California Water, and (3) the Tropical Surface Water; however, a large portion of transitional waters due to the mixing between the main water masses are also present [25]. Due to its position, where the Pacific Ocean joins with the GoC, the MCR is significantly influenced by large-scale processes such as the ENSO, which in its warm phase (El Niño) generates the advection of warm and oligotrophic water masses that decrease the levels of primary production, while during its cold phase (La Niña), it is related to increases in nutrient availability. Therefore, there is an increase in the phytoplankton production [26].

This study also includes the connection between the MCR and the Urias coastal lagoon [27], a waterbody with an “L” shaped geomorphology, a highly variable bathymetry, and an estuarine circulation during the rainy season and anti-estuarine during the dry season [28]. The mean salinity is 34 psu with the highest values (39.4 psu) during the drought season and the minimum (31.7 psu) during the rainy season [29]. Because it is a waterbody adjacent to Mazatlán harbor, one of the main harbors of the Mexican Pacific Ocean where heavy merchant and tourist ships converge, the connection area is continuously dredged to allow the safe entry of the vessels to the port [27]. Additional relevant economic activities, such as extensive aquaculture, also occur in the region.

2.2. Sampling

Two sampling expeditions were carried out in a boat with an outboard motor. The first expedition occurred on 23 and 24 August 2022, and the second occurred on 8 and 9 November 2022. A total of 23 stations were sampled in each expedition, including the MCR and its connection with the Urias coastal lagoon (Figure 1C). The geographical location of each station was reached with a GPS (Garmin 64sx). At each station, high-resolution hydrographic data (temperature (°C), salinity (psu), dissolved oxygen (mg·L⁻¹), and total dissolved solids (g·L⁻¹)) were acquired with a multiparameter sonde (YSI, model Pro 30) previously calibrated by the manufacturer. Additional water column information was considered in each sampling expedition, such as the Secchi disk’s depth/point of disappearance. Subsequently, surface water (at 2 m depth) was collected with a water sampler bailer (UWITEC, 5 L capacity). Immediately after collection, subsamples of 1 L were fixed on board with a Lugol’s acetate solution and kept in the dark until analysis.

2.3. Laboratory Analysis

Once in the laboratory, the samples were immediately analyzed after collection using the Utermöhl method, with the sedimentation of 50 mL columns, kept in the dark for 24 h [30]. The phytoplankton organisms were identified at the species level with a Carl Zeiss inverted microscope (Axiovert A1) following standard keys [31,32,33] as well as with specialized keys and catalogs specific for the Mexican Pacific and the GoC [34,35,36,37,38]. The identified species were compared and confirmed with international repositories (e.g., AlgaeBase, WORMS). Finally, the number of organisms was standardized to abundance units (cells L⁻¹) following standard procedures [30] by scaling the number of cells counted considering a smaller sample volume, in our case, 50 mL of the sedimentation columns, as mentioned above.

2.4. Data Analysis

Based on the identification of the species, diversity was calculated following the Shannon–Weaver index $H^{\prime }$ with the expression: $H^{\prime }=-\sum _{i=1}^n\left(p_{i}ln{p}_i\right)$, where $H^{\prime }$ is the diversity index, $p_i$ is the proportion of each group in the sample, and $ln{p}_i$ is the natural logarithm of this proportion [39]. Generally, $H^{\prime }$ is an index used worldwide because it considers aspects of both abundance and evenness of the taxa present in a region; then, $H^{\prime }$ usually increases with the number of taxa in the community structure [40].

We used the Mantel test to assess the congruence between the similarity matrices for the abundance of diatoms and dinoflagellates from the two contrasting datasets. This test performs a permutation of each element in a distance matrix to assess the goodness of fit between two multivariate datasets by permuting each element in a calculated matrix of dissimilarity indices to derive a distribution of correlation values [41,42,43,44]. The resulting R-statistic is similar to Pearson’s correlation coefficient (r); with increasingly similar dissimilarity matrices, the Mantel R-statistic will approach 1 [45]. We performed an additional Mantel test to examine the two contrasting seasons’ environmental variables.

3. Results

3.1. Hydrography

The hydrographic variables recorded during the sampling expeditions are summarized in Table S1, which showed marked variations between both sampling periods. The mean surface temperature in August was 30.9 °C; in November, it was 25.7 °C, representing a difference of 5.2 °C (Figure 2A). The mean surface salinity values showed variation with a concentration of 34.8 psu in August and 35.6 psu during November (Figure 2B); this slight variation can be attributed to the fact that during August, the rainy season occurs in the region, which slightly decreases salinity levels. The dissolved oxygen recorder at the surface also showed variations in both seasons with a mean value of 6.64 mg·L⁻¹ in August and 4.39 mg·L⁻¹ in November (Figure 2C). The mean values of the total dissolved solids at the surface were very similar in both samplings, with 34.74 g·L⁻¹, while in November, 35.06 g·L⁻¹ was recorded (Figure 2D). Finally, the Secchi depth in both seasons also showed variability, with mean values of 3.55 m in August and mean values of 4.79 m in November, which was attributed to the contribution of organic matter to the coastal zone due to freshwater discharge during the rainy season.

The horizontal distribution of these hydrographic variables also showed variations in time and space. During August, high temperatures (>30 °C) were observed practically in the entire sampling domain (Figure 3) (Figure 3A), while in November, changes were observed in the horizontal distribution of temperature with lower values (25 °C) in the region closest to the coast and higher values in the oceanic region (27 °C) (Figure 4A).

The horizontal distribution of the surface salinity values showed clear differences between both sampling periods; during August, values of 34.5 psu were observed in the region closest to the coast, in the connection of the Urias coastal lagoon with the sea, which were gradually increasing their value with >35 psu in the region furthest from the coast (Figure 3B), while in November, the salinity values were relatively homogeneous except for some cores of lower salinity observed in the oceanic portion of the study area (Figure 4B).

The horizontal distribution of the dissolved oxygen showed important variations during both seasons. In August, it ranged from 5.56 to 9.63 mg·L⁻¹, with maximum values recorded in the region closest to the coast, showing high concentration (>7 mg·L⁻¹) in the connection between the Urias coastal lagoon and the MCR and secondary high values observed farthest from the coast, which reaches values of 6 mg·L⁻¹ (Figure 3C). In November, the dissolved oxygen concentration ranged from 3.00 to 5.68 mg·L⁻¹ with a relatively homogeneous horizontal distribution throughout the study area (Figure 4C). Finally, the horizontal distribution of the values of the total dissolved solids was different with higher concentrations in November (Figure 3D and Figure 4D). In August, a small core of the highest concentrations was observed in the farthest part from the coast.

3.2. Phytoplankton Structure

The phytoplankton structure identified in this study presented changes between the two sampling seasons both in species richness and abundance.

During August, 232 species were identified, representing a total of 124,780 cells L⁻¹ (Table S2). The identified species were 125 diatoms (with a total abundance of 56,300 cells L⁻¹), 101 species of dinoflagellates (with a total abundance of 53,200 cells L⁻¹), 2 species of silicoflagellates (with a total abundance of 200 cells L⁻¹), 2 euglenoids (with a total abundance of 240 cells L⁻¹), 1 coccolithophore (with a total abundance of 80 cells L⁻¹) and 1 ciliate (with a total abundance of 14,760 cells L⁻¹).

Of the diatoms identified, Cylindrotheca closterium (Ehrenberg) Reimann & J.C. Lewin 1964 was the most abundant species, with 5680 cells L⁻¹, followed by Planktoniella sol (G.C. Wallich) Schütt 1892, which reached 4040 cells L⁻¹. The least abundant species included Pleurosigma normanii Ralfs 1861 and Roperia tesselata (Roper) Grunow ex Pelletan 1889, which barely reached 20 cells L⁻¹. Protoperidinium punctulatum (Paulsen) Balech 1974 was the most abundant dinoflagellate, with 6740 cells L⁻¹, followed by Lingulodinium polyedra (F.Stein) J.D. Dodge 1989, which reached 5520 cells L⁻¹. The least abundant species were Gyrodinium rubrum (Kofoid & Swezy) Y. Takano & T. Horiguichi 2004, Tripos gravidus (Gourret) F.Gómez 2013 and Gonyaulax diegensis Kofoid 1911 that reached 20 cells L⁻¹. Regarding the silicoflagellates identified, Dictyocha californica Schrader & Murray 1985 was the most abundant species with 160 cells L⁻¹. Euglena acusformis J. Schiller 1925 reached 220 cells L⁻¹ while the ciliate Mesodinium rubrum was observed with a high abundance of 14,760 cells L⁻¹.

The phytoplankton structure identified in November was quite different in terms of richness and abundance. This season, 225 species were identified, representing a total of 219,880 cells L⁻¹ (Table S3). The species listing included 120 species of diatoms, summarizing 105,200 cells L⁻¹, 97 species of dinoflagellates, which reached 95,640 cells L⁻¹, 4 species of silicoflagellates with 6320 cells L⁻¹, 1 species of a ciliate with 8640 cells L⁻¹ and 3 species of cyanophytes summarizing 4080 cells L⁻¹.

In terms of diatoms, Thalassionema nitzschioides (Grunow) Mereschkowsky 1902 was the most abundant species with 26,680 cells L⁻¹, followed by Tetramphora decussata (Grunow) Stepanek & Kociolek 2016 with 6320 cells L⁻¹, while Nitzschia leehyi G.Fryxell 2000, Lithodesmium variabile H. Tanako 1979, and Proboscia alata (Brightwell) Sundström 1986, among others, presented the lowest abundance with 20 cells L⁻¹. In terms of dinoflagellates, Protoperidinium punctulatum (Paulsen) Balech 1974 was the most abundant species, reaching 16,380 cells L⁻¹, which was followed by Gymnodinium catenatum with 10,100 cells L⁻¹, while Karenia brevisulcata (F.H. Chang) Gert Hansen & Moestrup 2000 and Karenia mikimotoi (Miyake & Kominami ex Oda) Gert Hansen & Moestrup 2000 presented the lowest abundance, with 20 cells L⁻¹. This season, Dictyocha fibula Ehrenberg 1839 was the most abundant silicoflagellate with 3580 cells L⁻¹. Trichodesmium hildebrandtii Gomont 1892 reached 2440 cells L⁻¹. Finally, the ciliate Mesodinium rubrum reached 8640 cells L⁻¹.

Some differences were identified when comparing the dominant species between each sampling period, particularly the differences between diatoms and dinoflagellates. For example, while the diatom C. closterium presented 5680 cells L⁻¹ in August, their abundance was 4260 cells L⁻¹ in November (Figure 5A). In contrast, while the diatom T. nitzschioides dominated in November with 26,680 cells L⁻¹, their abundance barely reached 20 cells L⁻¹ in August (Figure 5B). For the case of dinoflagellates, P. punctulatum was the dominant species in both sampling periods; however, while in August, their abundance reached 6740 cells L⁻¹, in November, it amounted to 16,380 cells L⁻¹ (Figure 5C).

Regarding the diversity index $H^{\prime }$, the values were high in both seasons with slight variations; in August, the calculated value was 4.20; in November, it was 4.07.

Finally, all Mantel tests performed between distance matrices showed no correlation between the two contrasting seasons. Concerning diatom abundance distribution, Mantel’s r was 0.4 (p < 0.05), while for dinoflagellates, Mantel’s coefficient was 0.1 (p = ns). These results show that diatom and dinoflagellate abundances, and community composition, significantly differed between the two contrasting seasons. In addition, tests performed between environmental variables showed no correlation between the distance matrices (Mantel’s r = 0.4; p < 0.05), suggesting that the environment significantly differs between the two contrasting seasons.

4. Discussion

The results presented here confirmed the high phytoplankton species richness that the MCR supports in high abundances, with a marked seasonal variability related to the environmental variables, particularly with the sea surface temperature. This variability between August and November could be attributed to the warming/cooling processes to which the region is subjected. During the warm season (August), radiation is at a maximum, the surface layer acquires a higher temperature, and, therefore, there is a marked stratification through the water column that blocks the flow of nutrients from the bottom toward the surface. Conversely, during the transitional period to the cold phase (November), the water column begins to lose heat, generating vertical convective movements that mix the water column, ensuring nutrients in the euphotic zone are available for the phytoplankton; additionally, during this season, the winds pattern begins to intensify, assisting the mixing along the water column [23]. Although we do not have measurements of the nutrient concentration during our observations and given the delayed reaction of the phytoplankton response to new nutrients, we assume this mechanism took place during November (even late October); this explains the high phytoplankton abundance observed, which showed a wide variation in August sampling.

But what could be the origin of the high species richness reported in this study compared to what was documented in previous ones? The answer could be in the oceanographic conditions during our observations. One of the uncertain aspects is the role ENSO events played in the MCR phytoplankton structure. It is important to note that the results presented here are framed in the context of a long and strong La Niña event, which may explain the high species richness found in the two seasons. For example, while previous studies have reported 76 phytoplankton species [10,11,12,13], our results listed 232 species, which could be related to the cooling and fertilization processes during La Niña. Recent research suggests that the concentration of chlorophyll-a (an indicator of phytoplankton biomass) in the MCR increases considerably during La Niña events, which is associated with a decrease in the sea surface temperature and an increase in the wind patterns that intensify the coastal upwelling of the region [23]. Coastal upwellings are one of the primary mechanisms that ensure the nutrient supply toward the euphotic zone due to the uplift of cold and nutrient-rich water masses benefiting phytoplankton communities, mainly the diatoms [46]; then, the coastal upwelling that is presented along the MCR could explain the differences found in terms of species richness between our study and previous ones.

In our samples, Tripos gravidus, which tends to be part of the shade flora (between 100 and 200 m depth), is perhaps signaling upwelling. However, much about ENSO dynamics and how they affect the phytoplankton species composition in the MCR remains undiscovered, so studies covering more seasons over different years are needed. Another factor that could explain the high number of species reported here is that the sampling effort (number of stations carried out in our study) was much higher than that applied in previous studies, where only a few stations were considered.

Some studies have documented the effect of La Niña events on phytoplankton communities in other domains of the Pacific Ocean. Indeed, the strong La Niña 2010–2011 impact on the phytoplankton composition in Australian waters was evaluated by Thompson et al. [47], who documented a dominance of diatoms over dinoflagellates, as was our case. A significant increase in diatom dominance associated with elevated marine productivity during La Niña 1998 was also documented in the Equatorial Pacific [48]. Similarly, the diatoms abundance in the western and central Pacific was considerably higher during La Niña 1999, reflecting the hydrographic conditions and the high nutrient concentration of the surface waters [49].

The MCR receives untreated sewage from different coastal discharges from the 500,000 population of Mazatlán city. It has been related to eutrophication processes and the generation of algal blooms, some of which are harmful. Algal blooms in the MCR are a recurring phenomenon that requires periodic monitoring and evaluation because toxic species produce some of them. In this study, high values of the ciliate Mesodinium rubrum were observed, particularly in August. This species has been previously reported as a cause of harmful algal blooms in the MCR [50] and in the southern GoC [51] related to the wind patterns of the region that induce upwelling processes. Generally, the blooms caused by this species are characterized by being short-lived (1–3 days) and present elongated patches parallel to the coast, which have been related to turbulence processes along the water column as a response to light exposure and the current circulation pattern [50]. In our case, the bloom observed during August could be related to the dredging of the navigation channel that allows deep-draft vessels (e.g., tourist cruises) to enter the port of Mazatlán because the navigation channel was being dredged the days before and during our sampling. Therefore, the turbulence generated by this process, the resuspension of sediment and organic matter, and the fact that the cells could have been exposed to better light conditions may explain the high density of organisms found. Blooms of this species in the MCR have been reported to reach even 2 × 10⁶ cells L⁻¹ [50], and although in our study, they only reached 14,760 cells L⁻¹, it can be considered a bloom.

Mesodinium rubrum is an organism that, being photosynthetic, releases oxygen into the water column. Some studies indicate that blooms of this species induce significant increases in the dissolved oxygen levels, particularly in the surface layers, even reaching supersaturation [52]. Then, in our case, the bloom observed in August could explain the increase in the dissolved oxygen levels (Figure 2C). Interestingly, the area with a high concentration of dissolved oxygen observed at the entrance of the Urias coastal lagoon in August (Figure 3C) is associated with the presence of this species.

In our study, Gymnodinium catenatum was another species observed with high abundances, particularly in November, reaching >10,000 cells L⁻¹. Blooms of this species have been reported in the specialized literature and are related to outbreaks of paralytic shellfish poisoning in the MCR [53]. Ramírez-Camarena et al. [54] analyzed the dynamics of the blooms of this species in the MCR during an annual cycle; their results showed that blooms occur in spring (April) and autumn (October) with a duration of 1 to 4 days and abundances of 5000 and 3873 cells L⁻¹, respectively.

Other planktonic populations reported in high abundance in the MCR are cyanobacteria of the genus Trichodesmium. For example, Cortes-Altamirano [55] reported blooms of the cyanobacterium Oscillatoria erythraea [now called Trichodesmium erythraeum], whose densities can exceed 600,000 cells. In our case, cyanobacteria were only found in November with three species, T. tenue Wille 1904, T. hildebrandtii, and T. thiebautii Gomont 1890. Although their abundance totaled 4080 cells L⁻¹, their presence provides evidence of the potential of the MCR to fix atmospheric nitrogen.

Diversity ($H^{\prime }$) was an indicator also found with high values (>4) in both seasons of our study with a slight variation between August and November attributed to the changes in the species richness [40]. These values are similar to those reported in previous works in the MCR and the GoC. Indeed, in the MCR, Alonso-Rodríguez et al. [15] reported values from 1.5 to 4.5 depending on the season. Values ranging from 2.5 to 4.2 have been reported in coastal regions on both sides of the gulf [56], while values from 1.4 to 5.8 have been reported in oceanic waters of the central and northern gulf [57,58]. Taken together, these $H^{\prime }$ values are considerably higher than those reported in other environments of the globe, confirming the high MCR diversity. For example, in the California Current System, maximum values of 2.3 have been reported [59]; in the Arabian Sea, the values reach 3.28 [60], while in the northwestern Mediterranean Sea, values up to 1.46 have been reported [61].

Finally, Mantel tests showed that diatom and dinoflagellate abundances and species composition significantly differed as they showed low correlation values. These differences in community structure could be related to the variations of the hydrographic variables between the two contrasting seasons. The Mantel test performed on environmental distance matrices also showed poor correlation.

5. Conclusions

The results presented here allowed us to confirm the high richness, abundance, and phytoplankton diversity that the MCR supports and suggest that some hydrographic variables, particularly the sea surface temperature, are directly related to changes observed in the community structure in both seasons considered in this study. The high number of species observed in this study, much higher than those reported in previous studies, could be related to the oceanographic setting of our observations in the context of a strong and long La Niña event, whose effects on the phytoplankton structure of the region have not yet been fully studied and understood. Likewise, the effect of many large-scale processes such as “the Blob” (the sudden overheating of surface waters that occurred in the Pacific Ocean between 2014/2015 [62]), heat marine waves, and the warm phase of ENSO (El Niño) and their relationship with phytoplankton organisms in the region have also not been fully evaluated. Moreover, recent studies suggest that these processes will be increasingly intense and recurrent in the Pacific Ocean and adjacent regions. There is a trend toward an increase in sea surface temperature and the proliferation of harmful algal blooms, particularly in the MCR. In this order of ideas, increasing the capacity for long-term multidisciplinary oceanographic monitoring is imperative to understand the causes and potential impact these processes could have on phytoplankton communities; this is also imperative in a context where the deterioration of coastal ecosystems because of anthropogenic pressures is becoming more evident. Therefore, the knowledge of marine biodiversity, mainly of the organisms located at the base of the trophic webs (in this case, phytoplankton), becomes necessary.

As final remarks, the taxonomic list presented here allowed us to identify interesting differences between each sampling period in a discipline whose nomenclature has been constantly changing in recent years. Our work involved conventional microscopy techniques applying methodologies that have been used in the last hundred years, as the Utermöhl method is still in use [63]; however, it is necessary to continue advancing using new techniques. Indeed, given today’s taxonomic schemes, scanning electron microscope observations and DNA analyses that confirmed species identification become necessary.