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INTRODUCTION
Macroalgae constitute a key marine community. This group embraces more than 40,000 species around the world, displaying high variability in physiology, morphology, and phylogenetic origin, as well as several key conditioning environmental and biological variables (e.g.,Guiry, 2012; Hurd et al., 2014). Communities vary strongly along the littoral zone and with latitude, as well as with seasonal and interannual variability (Gaspar et al., 2017; Cruz-Motta et al., 2020; Vélez-Rubio et al., 2021).
In coastal marine ecosystems, abundance estimates of different taxa are commonly made at spatial scales ranging from small (a few or hundreds of meters) to mesoscale (a few to hundreds of kilometers). At smaller spatial scales, many studies have linked community structure with variation in environmental factors (e.g., local oceanographic conditions, depth, sedimentation, pollutants) and species interactions (e.g.,Martins et al., 2013; Sangil et al., 2014, 2018).
Changes in the macroalgae community can be derived from changes in temperature, salinity, and light (Sangil et al., 2018) and changes in nutrient concentrations (Piñón-Gimate et al., 2012). Some green macroalgae such as Ulva and Caulerpa species, and red macroalgae such as Gracilaria spp. and Acanthophora spicifera (M. Vahl) Børgesen (Russell, 1992; McGlathery, 2001; Lapointe & Bedford, 2007), can grow inordinately in response to excessive anthropogenic derived nutrients (Valiela et al., 1997; Morand & Merceron, 2005), especially when water temperature conditions are favorable to their growth. Higher nutrient loads benefit opportunistic benthic algae and drift algae; besides soft-tissue filamentous algae are capable of quick uptake of nutrients and subsequent rapid increase in biomass, which leads to their domination in eutrophic systems (Pedersen & Borum, 1997; Valiela et al., 1997; Nelson et al., 2008). This has resulted in the formation of macroalgae blooms and green-tide events which have been reported in many parts of the world including Europe, North America, South America, Japan, and Australia (Fletcher, 1996; Morand & Briand, 1996; Hiraoka et al., 2004; Morand & Merceron, 2005; Merceron et al., 2007). Typically, macroalgae blooms are characterized by choking off waterways in the immediate area of the bloom and subsequently local wind and tide drives senescent algae to the shore, that can change coastal marine habitats through eutrophication (Valiela et al., 1997) and can cause economic losses to marine industries (e.g., fisheries and tourism) (Nelson et al., 2008; Liu et al., 2013).
The Gulf of California (GC) is a semi-enclosed sea on the Pacific coast of Mexico and one of the most biologically diverse marine areas in the world. In La Paz Bay, South Baja California, changes were reported depending on site and seasons for example, Sargassum species and Spyridia filamentosa (Wulfen) Harvey were the most abundant species during spring, and one of the sites with the highest biomass was El Malecón during winter and Punta León during summer (Casas-Valdez et al., 1997); while Cruz-Ayala et al. (1998) reported that species from the genus Sargassum, Spyridia filamentosa, Caulerpa sertularioides (S. G. Gmelin) M. Howe, Padina durvillei Bory, and Hydroclathrus clathratus (C. Agardh) M. Howe, were the most abundant species and in total represented 75% during an annual cycle. In a latter study in the same bay, high biomasses of Ulva species were found; in some areas and especially in the waterfront of La Paz City, the biomass of this taxon showed an important increased after a hurricane event, where the biomass collected in the beach ranged from 350 to 540 g m-2. The peaks in biomass were attributed to the runoff from rainfall which carried nutrient rich waters and to the increase of pebbles due to water motion after the hurricane (Aguila-Ramírez et al., 2005).
In a recent study, changes in macroalgae biomass during a one-year period, in different sites of La Paz Bay, were presented along with the evaluation of the trophic state, that was mostly oligotrophic, while macroalgae biomass was reported below 200 g m-2 wet weight for the important species found (Antonio-Robles et al., 2021). The aim of the present study was to identify the macroalgae species that contribute the most to the biomass of macroalgae blooms of La Paz Bay at different sites and to identify if their abundance was related to some physicochemical parameters in different sites of the bay with different characteristics in a two- year cycle.
MATERIALS AND METHODS
Study area
La Paz Bay is the largest water body in the eastern coast of the Baja California peninsula, in the Gulf of California, with an approximate surface of 1200 km2. lt is located at 24º06’ and 24º47’ N, 110º18’ and 110º45’ W. Its approximate dimensions are of 80 km long and 35 km wide, it is separated from the gulf by a narrow peninsula, projected to the north and the insular complex Espiritu-Santo-La Partida. Therefore, the connection with the gulf occurs trough two openings, la Boca Grande which is deep, located to the north, and the San Lorenzo Channel narrow and shallower, located east. The bay presents a bathymetric gradient with depths of 10 m to the south, to 450 m in the north portion, where the Cuenca Alfonso is located.
Ensenada de La Paz (24°06’ - 24°11’ N, 110°19’ - 110°26’ W), is the lagoon formed by the very large sand spit at the southern end of the La Paz Bay (Fig. 1). The inlet is 1.2 km wide, 4 km long and 7 m deep. At mean sea level, the surface area of the lagoon is approximately 45 km2. The lagoon is shallower than the inlet; with depths from 2 to 6 m. The tide regimen is a mixed semidiurnal type (Obeso-Nieblas et al., 1993).
The climate is arid dry (BWh), the annual evaporation (215 mm) exceeds annual precipitation (180 mm); the maximum rainfall in the bay occurs between July and October, associated with southeast winds, tropical storms, and hurricanes (Obeso-Nieblas et al., 2008); but dominant winds come from the northwest from November to March. The annual average temperature is 24.6°C; the minimum average temperature is 14.8°C that occurs in winter and the maximum is 32.6°C in summer (INEGI, 2017).
In the bay, in a previous field trip (2009), all the shallow areas of the bay were visited, and four sampling locations were chosen considering excessive presence of some benthic macroalgae species near the shore that were then considered as one macroalgae bloom. Each site presented different characteristics (Fig. 1). Site Playa Conchalito (Co): this site is located south of the ensenada and of the other sites. It is in the vicinity of the city and at the time of the sampling period it had no influence from anthropogenic activities; however, a drain presumably for rainfall waters discharges directly at this site. The bottom sediment consists mainly of sand and some pebbles, also some rocks and shells that serve as substratum for macroalgae. Average depth for this site is 0.5 m. when there are dead tides. Site Plaza Vista Coral (VC): it is located at one side of the Marina Cortez, despite of being in proximity of the marina at the time of the sampling period it had no influence directly from the restaurants or water activities at this site. The bottom is characterized by the presence of rocks as substratum and soft sediments that sometimes had bad odor. At this site we could also find seagrasses that serve as a substratum and anchoring for some of the Ulva species. Average depth for this site when the tides are dead is 1m. Site Casa del Marino (CM): this site is located at the north of the ensenada, adjacent to the tidal channel in front of the city of La Paz. It is protected and shallow and has a soft surge. Since this location has been affected by anthropogenic activities, the natural substratum has been modified and inorganic and organic material has been added. The sandy bottoms are covered in part by some boulders, shells, and coral remains. A rock breakwater was built to further moderate the surge. Average depth when dead tide is 1.5 m. Site Enfermeria (En): this site is located across the highway and the mangrove, its influenced by the bay waters, it is located near a crossroad, this beach is visited regularly by local people. This is a very shallow beach with sandy bottom with boulders. Average depth when dead tide is less than 0.5 m. These sites were sampled one time during two years at each of the following months: February, April, June and October of 2010 and February, April, July and October of 2011.
Environmental variables
At each site or macroalgae bloom, water samples were taken in the middle of the bloom and close to the edges during low and high tides. Temperature and salinity were determined in the field using a handheld multi-probe meter (YSI 556-Rickly Hydrological, YSI, Yellow Springs, USA) (ns4). Water samples (3 replicates) were frozen and taken back to the laboratory for further determination of nutrients: dissolved inorganic nitrogen (DIN), TN, DP, and total phosphorus (TP). Techniques used were those recommended by Strickland & Parsons (1972) and Grasshoff et al. (1983). Finally, the N:P ratio was obtained. Normality (Kolmogorov-Smirnov test) and variance homogeneity (Cochran’s test) were tested. A MANOVA analysis model was used to determine significant differences in seawater temperature, salinity and nutrients using date and site as independent variables. Means comparisons were carried out using Tukey’s test only when there was a significant effect of the interaction (P<0.05) (Zar, 1984).
Macroalgae biomass
At each site or macroalgae bloom, to obtain macroalgae biomass, replicate transects were laid out perpendicular to the coast according to the area covered by the bloom, with one transect at each end and the other in the middle of the bloom. In total, there were three transects through each bloom in each season of the year. For each transect, five equidistant points were defined (since the area covered by the bloom was very extensive), with end points at the shoreline and at the far edge of the bloom. At each point, macroalgae were collected from four, non-overlapping, randomly placed quadrants (0.25 m2) to estimate a square meter at each point. Samples were washed in the field with water from the lagoon and the species were separated by hand. Only species with biomasses >1 g m-2 were weighed with a digital balance (0.5 g). However, only species that contributed with more than 1% of the biomass were considered bloom forming and designated as “important” species, which were considered for analyses of species composition and temporal changes. A sample of each species was fixed with 4% formaldehyde-seawater solution for further determination at species level in the laboratory using as a reference work Setchell & Gardner (1924), Abott & Hollenberg (1976) and Chávez-Sánchez et al. (2019). Species names were revised in Guiry & Guiry (2022).
To describe the occurrence of “important” species during the surveys, total biomass was obtained as the sum of the biomass sampled. Relative abundance (RA) was obtained as the percentage of the biomass (B) contribution of each species (j) to the total biomass of the species sampled (j =1 to s).
For each sampling trip, the mean biomass of each species (MBj) was calculated as the sum of the biomass per square meter (b=1 to 15) and divided by the total number of points sampled (p = 15) at each macroalgae bloom.
The mean biomass of each species at each site was expressed as g m-2 of wet weight (WW) and plotted monthly for each macroalgae bloom. For each month, biomass data was used to describe changes within and between macroalgae blooms.
The relationships between environmental parameters and “important” species biomass with the highest presence were analyzed by principal component analysis (PCA) (Sfriso & Marcomini, 1997). The significance criterion for each component was the eigenvalue (1). The greatest absolute values were selected from the correlation matrix. If there were two or more values in the same column, there was a correlation, if the signs were the same there was a direct relation, and if the signs were different there was an inverse correlation (Ballesteros-Grijalva et al., 1996). All analyses were carried out using the program STATISTICA (StatSoft, 2004).
Results
Environmental variables
Temperature showed significant differences during the sampling period with the lowest temperature at Co during February 2011 (17.5° C) and the highest at En during June 2011 (32.7° C), an annual pattern could be observed (Fig. 2a). Salinity showed little variation, but significant higher values (p < 0.05) were recorded during February (38.5 to 40.5) and April (38.5 to 40.0) at the four sites during 2011 (Fig. 2b).
Figure 2 Environmental parameters: a) Mean temperature (±SD), b) mean salinity (±SD), by year, month, and site. Co=Conchalito, VC= Vista Coral, CM= Casa del Marino and En=Enfermería.
Nutrient concentrations were variable along the study period, between years, months, and sites. For the DIN significant differences were found (p < 0.05), the highest DIN was recorded during 2011 at sites VC and Co during June, no clear seasonal pattern could be observed (4.2, 3.8 and 3.6 µM l-1; respectively; Fig. 3a). Total nitrogen concentrations between years, months, and sites, were also variable but with no significant differences; however, the highest concentration was observed during 2010 at VC during February (52.4 µM l-1, Fig. 3b). For the PO4-3 no clear seasonal patterns could be observed (Fig. 3c). The TP concentrations were variable but were very low, only during 2010 the highest concentration was observed at En in February (2.8 µM l-1); however, no clear seasonal patterns could be observed (Fig. 3d).
Biomass
During the two-year sampling period 9 macroalgae species were identified as “important”: 4 species belonging to the Phylum Rhodophyta, 5 species belonging to the Phylum Chlorophyta, plus one unidentified cyanoprokaryotic species (Table 1). In general, during the study the highest biomass found corresponded to the red species Acanthophora spicifera, followed by the green Caulerpa verticillata J. Agardh and the red Spyridia filamentosa (Table 1).
Table 1 Total and relative biomass of “important” species present in macroalgae blooms in La Paz Bay.
| Species | Total Biomass (g) | Relative biomass (%) |
| Acanthophora spicifera (M. Vahl) Børgesen | 60121.48 | 46.50 |
| Caulerpa verticillata J. Agardh | 13099.2 | 10.13 |
| Spyridia filamentosa (Wulfen) Harvey | 12399.8 | 9.59 |
| Ulva ohnoi M. Hiraoka & S. Shimada | 9153.34 | 7.08 |
| Caulerpa sertularioides (S. G. Gmelin) M. Howe | 7883.6 | 6.09 |
| Ulva sp.1 | 5198.5 | 4.02 |
| Halimeda discoidea Decaisne | 4759.3 | 3.68 |
| Gracilaria vermiculophylla (Ohmi) Papenfuss | 4031.3 | 3.11 |
| Cyanoprokaryotic species | 3685.9 | 2.85 |
| Laurencia pacifica Kylin | 2681.2 | 2.07 |
Differences in species presence and biomass were found between years, months, and sites. At site Co, the contribution of the biomass was made by four out of ten “important” species. Depending on the year and month biomass, composition changes were observed for this site. The most abundant alga for this site was the cyanoprokaryotic species in October 2010 (131.8 g m-2; Fig. 4). For site VC, nine out of ten “important” species were found. The speciesA. spicifera was the most important in 2010 and 2011, during June and October its biomass was higher than the rest of the species (Fig. 4). At CM we also found a high species composition (nine out of ten species) as well as the highest biomass. The speciesA. spicifera showed the highest biomass during the time the surveys lasted. During 2010 the highest biomass of A. spicifera was found during February and June (612.18 and 565.59 g m-2, respectively), while during 2011 the highest biomass was found during April (350.52 g m-2; Fig. 4).Caulerpa verticillata was found only at this site, its biomass was higher during June 2011 (266.17 g m-2; Fig. 4). At En only four species and the cyanoprokaryote were found. The speciesS. filamentosa was the most important species during both years, its highest biomass was found during June 2010 and October 2011 (139.9 and 187.32 g m-2; Fig. 4,y Fig. 5).
Figure 4 Seasonal variation in the mean biomass of important species at four sites. Co=Conchalito, VC= Vista Coral, CM= Casa del Marino and En=Enfermería. Cy= Cyanoprokaryote, Gv= Gracilaria vermiculophylla, Sf= Spyridia filamentosa, Uo= Ulva ohnoi, Usp1= Ulva sp.1, As= Acanthophora spicifera, Cs= Caulerpa sertularioides, Cv= Caulerpa verticillata, Hd= Halimeda discoidea, Lp= Laurencia pacifica.
Figure 5 Principal Component Analysis (PCA) for the correlation between macroalgae biomass and environmental parameters and nutrients. T=Temperature, Sal = Salinity, DIN= Dissolve Inorganic, TN= Total Nitrogen, PO4-3= Orthophosphates, TP= Total Phosphorus, Gv= Gracilaria vermiculophylla, Sf= Spyridia filamentosa, Uo= Ulva ohnoi, Usp1= Ulva sp.1, As= Acanthophora spicifera, Cs= Caulerpa sertularioides.
Biomass and environmental variables
Principal Component Analysis could only be performed with “important” species but that were also present during several months and sites. The eigenvalues showed that components 1 and 2 were the ones that could explain the correlations found (2.98 and 1, respectively). Component 1 explained 49.77%, while component 2 explained 30.11%. In component 1 it was observed that the biomass of A. spicifera and G. vermiculophylla was related with the DIN and PO4-3, and salinity. While in the component 2 G. vermiculophylla and Caulerpa sertularioides were related to TN and TP concentrations. The biomass of Ulva ohnoi M. Hiraoka & S. Shimada was not related to nutrient concentrations or any of the other parameters (Table 2).
Table 2 Factor contribution of environmental variables and species biomass. Gv= Gracilaria vermiculophylla, Sf= Spyridia filamentosa, Uo= Ulva ohnoi, Usp1= Ulva sp. 1, As= Acanthophora spicifera, Cs= Caulerpa sertularioides.
| Factor 1 | Factor 2 | |
| T | -0.594761 | -0.355900 |
| Sal | 0.895701 | -0.210119 |
| DIN | 0.895857 | 0.412315 |
| TN | -0.625975 | 0.656188 |
| PO4 | 0.635076 | 0.633119 |
| TP | -0.482226 | 0.796656 |
| *Gv | 0.542017 | 0.775922 |
| *Sf | 0.275897 | 0.126783 |
| *Uo | 0.294979 | -0.949220 |
| *Usp1 | 0.150411 | 0.105347 |
| *As | 0.724848 | -0.259063 |
| *Cs | 0.353115 | 0.691660 |
DISCUSSION
In La Paz Bay, 9 macroalgae species and one cyanoprokaryote were considered bloom forming species, which was like that number recordered for the southeast portion of the Gulf of California; where C. sertularioides, Ulva species, S. filamentosa and Gracilaria species were “important” macroalgae (Piñón-Gimate et al., 2008). These macroalgae have the characteristic of being ephemeral species, of rapid growth as previously reported in other regions of the world where macroalgae blooms are of importance (Piñón-Gimate et al., 2012). These species are also consistent with genera previously reported as bloom-formers in nutrient-rich coastal waters. Fletcher (1996) reported Caulerpa, Ulva, Gracilaria, and Hypnea as characteristic of eutrophic waters and cyanoprokaryotes under anaerobic conditions and low pH, also important components of macroalgal blooms (Lotze & Schram, 2000; McGlathery, 2001).
In general, the mean values of monthly biomass for the important species were lower than those previously reported for species in macroalgal blooms with nutrient enrichment from anthropogenic sources (Ochoa-Izaguirre et al., 2002; Scanlan et al., 2007). However, they were consistent with biomass values of communities in the Gulf of California (Cruz-Ayala et al., 1998; Casas-Valdez et al., 2000; Carballo et al., 2002).
The most abundant species was the red algae A. spicifera; it has been reported that this species shows high biomasses in places where it has been found as invasive, such as in the Hawaiian Islands where its biomass surpassed over the benthic communities after being introduced unintentionally (O’Doherty & Sherwood, 2007). However, A. spicifera had previously been reported in La Paz Bay, but it was only reported as present (Ávila et al., 2012). In a recent study its presence and abundance were described at some sites of La Paz Bay (Antonio-Robles et al., 2021), but its biomass was lower than that found in the present study (16.8 g m-2 and 43.1 g m-2, in 2017 and 2018, respectively). As it has been mentioned before conditions of the substratum of some of the sites, had changed over the years towards a sandier and muddier bottom (personal observation), hence the changes in the biomass observed trough could be explained in terms of a lack of substratum since activities remain the same such as in CM.
The green algae C. sertularioides was studied in Balandra where after a hurricane its biomass increased significantly; however, it latter disappeared from this site at La Paz Bay (Scrosati, 2001). Other studies have reported the presence of C. sertularioides associated with nutrient rich waters in coastal lagoons of Sinaloa in the Gulf of California (Piñón-Gimate et al., 2008). In the present study C. verticillata was abundant, it had also been reported in another sites, Esterito and La Concha, (Pérez-Estrada et al., 2013); however, in the most recent study in CM this species was not reported (Antonio-Robles et al., 2021), probably conditions, such as lack of substratum, were not favorable for this species at this site. Although there are no obvious answers as to whether this species was no longer present at CM, it shows that the presence of certain species depends not also on seasonal factors but also could be related to changes in the substratum as pointed out previously.
The PCA showed that the species A. spicifera and G. vermiculophylla were related with nutrient concentrations, and salinity; and in the other component G. vermiculophylla and C. sertularioides were more related with nutrient concentrations. While U. ohnoi showed no relation with the increases in nutrient concentrations, but also with none of the other parameters, hence its presence at this time must be related to some other factor, or the conjunction of several parameters. It has been shown that the species C. sertularioides was related to the ratio N:P in coastal lagoons of Sinaloa suggesting that high concentrations of nitrogen relative to low phosphorus levels favor its growth (Ochoa-Izaguirre et al., 2002; Piñón-Gimate et al., 2008).
In the region of the present study, Ulva species were the most abundant green algae in Laguna San Ignacio (Nuñez-López & Casas-Valdez, 1998). This abundance was related to the lower temperatures prevailing during the winter and to nutrient enrichment, although the authors did not measure nutrient concentrations. In La Paz Bay, other studies have found higher biomasses of Ulva from 351 to 537 g m-2 (Aguila-Ramírez et al., 2005), while in the present study the maximum biomass was of 138 g m-2. Biomass of these species was found at sites where nutrient loads are considered of importance even though sources are not recorded or reported to the municipal authorities. Biomass of Ulva was lower than that found at coastal lagoons of Sinaloa (Piñón-Gimate et al., 2008) and in general lower than Ulva beds of the Gulf of California (see Piñón-Gimate et al., 2012). Sfriso & Marcomini (1997) reported biomass production of Ulva of 2.4 kg m-2 DW in Venice lagoon, Italy in association with the nutrient loads of anthropogenic origin. The monitoring of macroalgae blooms is of importance given that continuous changes are occurring at coastal areas given the increase in population and anthropogenic activities.
