Hydrobiologia 501: 207–214, 2003. © 2003 Kluwer Academic Publishers. Printed in the Netherlands.
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Spatial and seasonal variation of macroalgal biomass in Laguna Ojo de Liebre, Baja California Sur, Mexico R. N. Aguila Ram´ırez, M. Casas Valdez, S. Ortega Garc´ıa, R. A. N´uñez L´opez & M. B. Cruz Ayala Laboratorio de Macroalgas. Centro Interdisciplinario de Ciencias Marinas. Av. Instituto Polit´ecnico Nacional s/n. Apartado Postal 592, La Paz, B.C.S., C.P. 23090, Mexico E-mail:
[email protected] Received 3 October 2000; in revised form 19 May 2003; accepted 20 June 2003
Key words: seaweed, biomass, spatial, seasonal, Ojo de Liebre, M´exico Abstract Laguna Ojo de Liebre is part of ‘El Vizcaíno’ Biosphere’s Reserve, one of the largest protected natural areas in the world. The contribution of seaweeds to the lagoons’ total biomass had not been previously quantified. The purpose of this study was to evaluate the spatial and temporal variations of seaweed biomass in the lagoon. Seaweed samples were taken every season during 1995 at six sampling stations distributed throughout the lagoon. Total specific biomass of seaweeds was at its peak in the summer, and minimum in spring. The highest total annual biomass was found at Isla Brosa in the lagoon’s central portion, and the lowest in El Dátil at the head. The seasonal and spatial variation of biomass in the lagoon is related with species richness and environmental parameters. Potentially important species in terms of biomass, wide spatial and temporal distribution, and potential use were: Spyridia filamentosa, Entheromorpha clathrata, Dasya baillouviana, Hypnea valentiae and Sargassum sinicola. Using PCA three groups of stations were defined: one chiefly at the lagoon’s mouth, another comprised the islands in the central portion, and the last in the lagoon’s head. Introduction Algae occupy an important place in marine ecosystems as primary producers and potential resources. Although some species are found in exploitable quantities, it is necessary to determine their presence, distribution, and abundance as a prerequisite to use them rationally. Mostly a result of its large latitudinal variations, the Baja California Peninsula comprises a great diversity of environments, among them the ‘El Vizcaíno’ Biosphere’s Reserve, one of the largest protected natural areas in the world which includes the Laguna Ojo de Liebre. Studies of marine algae in this lagoon are scarce. E. Y. Dawson collected specimens of marine algae sporadically during the Allan Hancock Pacific Expeditions to the Mexican Pacific between 1944 and 1963; he reported 41 different species. More recently, Aguila et al. (2000) described the macroalgal community in terms of species composition, spatial and temporary variations and species richness.
Seasonal cycles of seaweed biomass have been reported to occur in temperate (Chock & Mathieson, 1983; Kornfeldt, 1984; Scrosati, 2001), subtropical (Pacheco et al., 1992, 1999) and tropical areas (Cruz et al., 1998; Scrosati, 2001). However, little is known for the Baja California Peninsula’s western coast (Hernández et al., 1991; Nuñez & Casas, 1998), particularly in the case of its middle portion (Laguna Ojo de Liebre) where no evaluation of the seasonal variations in seaweed biomass has been undertaken to date. This study assesses the spatial and temporal variations in algal biomass in a semitemperate antiestuarine enviroment.
Description of sites studied Laguna Ojo de Liebre is located to the north of Baja California Sur, between 27◦ 35 –27◦ 55 N and 113◦ 58 –114◦ 20 W (Fig. 1). It comprises approximately 36 600 ha and is connected to the Sebastián Vizcaíno bay. This lagoon is hypersaline as it does
208 El Dátil It is also found northward of the lagoon, near the mouth. The substrate is sandy with scattered sandstone areas, and the average depth is 1 m. There are heaps of shells along the beach, as well as pebbles in some areas. Isla Brosa It is located to the center of the lagoon. It is the lagoon’s largest island, comprising an extension of 500 ha. It is formed by two portions of land linked by a marsh that crosses it from north to south. The substrate is mostly rocky, with some sandy zones. The average depth is 3 m. Isla Piedra Norte It is also located to the center of the lagoon. The water retreats approximately 200 m from the high water mark during ebb tides. The substrate is mostly pebbles, with some thick sand in shallower zones. The average depth is 1.5 m. Isla Piedra Sur Also located to the center of the lagoon, it presents a rocky substrate with a depth of up to 6 m. Campo Ejidatario Figure 1. Study area and sampling stations.
not receive any freshwater and there is a high degree of evaporation caused by the combined effect of wind and solar radiation. For this reason and the slow water circulation, Ojo de Liebre is considered to be an antiestuarine lagoon. The sampling stations located throughout the lagoon are briefly described below (Fig. 1).
La Hielera It is located to the north of the lagoon, near its mouth. The substrate is predominantly sandy, with an average depth of 0.7 m. There are shells, sandstone and pebbles striping along the beach.
It is located at the northwest of the lagoon’s head. It is a very shallow location, with a average depth of 0.4 m and a muddy-sandy bottom.
Materials and methods Sampling stations were located near the lagoon’s mouth (La Hielera and El Dátil), to the center (Isla Brosa, Isla Piedra Norte, and Isla Piedra Sur), and the head (Campo Ejidatario). These locations encompass most of the different environments within it (Fig. 1). To note, no samples were taken at Isla Brosa in the winter because adverse weather conditions made it impossible to approach the area. Algal samples were collected seasonally during 1995 (February = winter, May = spring, September = summer, November = autumn) at six stations.
209 At each station, samples were collected from the intertidal and subtidal zones, using a 200 m transect placed perpendicularly to the coastline as a guide. These distance was chosen because the maximum distribution of algae is found here. Samples were collected manually by snorkeling and SCUBA diving at 10 m intervals along the transect. A 1 m2 quadrat was used as sampling unit to estimate algal biomass. This quadrat size has been shown to be the best for obtaining a good sample of the species present and their biomass (De Wreede, 1985; Vázquez & González, 1995). Samples were fixed in a 4% solution of formaldehyde in seawater. In the laboratory, the seaweeds collected from each sampling unit was separated for identification and its weight determined to the nearest 0.1 g using an electronic balance. Environmental variables Surface water temperature at each sampling station was recorded with a thermometer (±0.1 ◦ C). Water samples were taken to determine salinity using the Knudsen method (Grasshoff, 1983). Depth was measured with a depth-meter. The type of substrate was determined by granulometric analysis (Folk, 1974).
using the Statgraphics Plus 2.0 statistical program (Statistical Graphics Corp., 1996).
Results Environmental variables The maximum average temperature (25.5 ◦ C) and salinity (39‰) occurred in the summer, whereas minimum figures were recorded in the winter when these dropped to 18 ◦ C and 35 ‰, respectively. Stations near the mouth (1 and 2) presented a sandy substrate, with low temperatures (19.8 ◦ C, 20.4 ◦ C) and low salinities (35.3‰, 35.5‰). This area is largely influenced by currents. The central portion of the lagoon (stations 3, 4 and 5) is characterized by the presence of islands where a rocky substrate prevails. The average temperature varies between 20.5 ◦ C and 20.7 ◦ C, and salinity ranges from 36.6‰to 36.4‰. The head of the lagoon (station 6) is shallow, sandy and muddy, and presents high temperatures (21.6 ◦ C) and a very high salinity (38.1‰) due to sun exposure and a relatively still water. Species richness
Species richness The number of seaweed species present in any given sampling station and season was determined. Seasonal and spatial variation in biomass For each of the species identified, and for the general analysis of wet biomass data, we used the terms defined for Cruz et al. (1998). The Kolmogorov–Smirnov test showed that biomass data did not follow a normal distribution (d = 0.37038; p < 0.01). Therefore a Kruskal–Wallis test (Zar, 1984) was performed separately on data for season and for locations, to test whether biomass varied significantly on a seasonal and/or spatial bases. Using the total annual seaweed biomass and the figures for environmental variables (temperature, salinity, depth, and substrate), a principal components analysis (PCA) was conducted. The purpose of this analysis was to obtain a small number of linear combinations of the five variables which account for most of the variability in the data, aiming to define locations sharing similar characteristics. To this end, variables were first standardized, then the PCA was performed
Total species richness for each sampling station is shown in Figure 2. Species richness for each sampling station and season is presented in Table 1. Isla Brosa (3) was the station with the highest species richness, followed by Isla Piedra Norte (4) and Isla Piedra Sur (5). The lowest species richness was found in La Hielera (1). The maximum species richness occurred in the summer, and the minimum in spring. Each sampling station displayed a particular seasonality pattern. Seasonal and spatial variations in biomass Seasonal variations in the biomass of those seaweed species with a relative annual biomass higher than 0.5% are listed in Table 2. Seasonal and annual biomass figures are expressed as g m−2 , and relative biomass numbers are given as percentages. The seasonal average biomass (SAB) was significantly different (H(3,456) = 38.8; p < 0.05) among seasons (Fig. 3). The maximum total seasonal biomass (TSB) occurred in the summer (87.8 g m−2 ), and the minimum in the spring (31.84 g m−2 ) (Table 2). As regards the spacial variation in biomass across the lagoon, the highest biomass throughout the annual
210
Figure 2. Spatial and seasonal variation of average biomass of seaweed, and spatial variation of species richness in Laguna Ojo de Liebre. Table 1. Species richness in Laguna Ojo de Liebre, B.C.S.
Winter Spring Summer Autumn
La Hielera
El D´atil
Isla Brosa
Isla Piedra Norte
Isla Piedra Sur
Campo Ejidatario
Total
4 0 0 0
3 0 5 0
0 0 24 26
16 20 26 14
7 0 9 16
5 4 11 13
25 23 42 41
Figure 3. Seasonal average biomass (SAB) in Laguna Ojo de Liebre.
cycle was recorded at Isla Brosa (3) (80 g m−2 ), followed by Isla Piedra Norte (4) (76.6 g m−2 ), and the lowest at El Dátil (2) (11.3 g m−2 ) (Fig. 2). The differences among stations were significant (H(5,454) = 131.38; p< 0.05). Seasonal biomass figures for the different stations are depicted in Figure 2. Seasonally, significant differ-
ences in average biomass between sampling stations were found in the spring (H(5,114)= 77.32; p < 0.05), summer (H(5,114)= 84.03; p< 0.05), autumn (H(5,114)= 46.47; p < 0.0.5), and winter (F(4,95)= 16.00; p < 0.05). In the spring, a large difference was found among stations because no seaweeds were present at La Hielera, El Dátil, Isla Brosa, and Isla Piedra Sur. The average biomass was 30.1 g m−2 at Isla Piedra Norte (4) and 1.8 g m−2 at Campo Ejidatario (6). The maximum variation in average biomass among these stations occurred in the summer. At Isla Piedra Sur (5) values were approximately 1 g m−2 , whereas at Isla Brosa (3) the average biomass was 55.5 g m−2 . In the autumn, the significant difference was due to the absence of seaweeds at La Hielera (1) and El Dátil (2). The species with the highest annual relative biomass (ARB) throughout the year were Spyridia filamentosa (17.1%), Polysiphonia pacifica (7.9%), Acrosiphonia saxatilis (6.4%), Sargassum sinicola (6.0%), Hypnea valentiae (5.9%), Enteromorpha clathrata (5.0%), Chondria dasyphylla (4.7%), Ectocarpus commensalis (4.7%) Polysiphonia scopulorum (4.6%)
211 Table 2. Biomass of seaweed in the Laguna Ojo de Liebre (g m−2 )
Acrosiphonia saxatilis (Ruprecht) Vinogradova Amphiroa beauvosii Lamouroux Caulerpa vanbosseae Setchell et Gardner Chaetomorpha linum (Müller)Kützing Chondria dasyphylla (Woodward) C.Agardh Codium cuneatum Setchell et Gardner Codium simulans Setchell et Gardner Colpomenia sinuosa Derbes et Solier Colpomenia tuberculata Saunders Corallina vancouveriensis Yendo Dasya baillouviana (Gmelin) Montagne Ectocarpus commensalis Setchell et Gardner Enteromorpha clathrata (Roth) Greville Enteromorpha intestinalis (Linnaeus) Ness Enteromorpha prolifera (Müller)J.Agardh Gracilaria pacifica Abbott Hydroclathrus clathratus (C.Agardh) Howe Hypnea valentiae (Turner) Montagne Jania adhaerens Lamouroux Laurencia clarionensis Setchell et Gardner Laurencia pacifica Kylin Laurencia snyderiae Dawson Osmundea crispa (Hollenberg) Nam. Polysiphonia pacifica Hollenberg Polysiphonia scopulorum Harvey Polysiphonia simplex Hollenberg Sargassum sinicola Setchell et Gardner Spyridia filamentosa (Wulfen) Harvey Ulva lactuca Linnaeus TSB= 250.23
SB W
SRB %
SB S
SRB %
SB Su
SRB %
SB A
SRB %
TB Annual
ARB %
0.5
0.9
0.1
0.2
4.3
13.4
0.02
0.04
0.3 18.1 3.4 0.2 1.0 1.13
0.14 4.29 3.38 7.32 7.17 0.92
1.55 0.10 1.51
4.87 0.30 4.74
0.7 1.2 2.1 0.1 2.6 1.6 6.4 7.40 3.13 0.96 0.90 6.75 7.69
0.3 14.0 2.6 0.2 0.8 0.88
0.08 2.28 1.79 3.88 3.80 0.49
0.6 1.0 1.8 0.1 2.3 1.4 8.2 6.5 2.75 0.84 0.79 5.93 6.75
2.8
0.5
22.7 1.4 0.6
2.2
0.3
7.2 0.4 0.2
0.05
0.16
0.01 0.69 0.01 2.88
0.03 2.17 0.02 9.05
0.38 5.62 0.85
0.49 7.23 1.09
8.18 1.70 14.2 4.15
3.24
10.1
0.04 1.89 1.46 2.72 0.71 3.26 0.08 0.92 2.05 15.1 2.45 4.23 0.17 19.2 1.79
2.45 1.55 1.85 3.93 1.61 2.65 1.45 0.37
2.61 0.54 4.53 1.32
0.04 1.66 1.28 2.39 0.62 2.86 0.07 0.81 1.80 13.3 2.15 3.71 0.15 16.9 1.57
1.90 1.20 1.44 3.05 1.25 2.06 1.13 0.29
5.33 0.11 2.38 0.46 15.3
6.86 0.14 3.07 0.59 19.7
34.8 3.5 4.4 14.3 25.7 3.2 12.9 14.78 2.75 8.29 10.55 25.31 27.08 14.02 2.73 5.82 3.86 31.95 10.61 8.61 24.62 3.08 14.64 42.66 25.20 15.81 32.54 92.95 3.36
6.4 0.6 0.8 2.6 4.7 0.6 2.4 2.73 0.51 1.52 1.95 4.66 4.99 2.58 0.50 1.07 0.71 5.89 1.96 1.59 4.54 0.57 2.70 7.86 4.65 2.91 6.00 17.13 0.62
9.18 2.23 0.73 2.40 0.18
17.33 4.20 1.37 4.53 0.33
2.30 0.60 0.01 11.00 9.72
4.34 1.13 0.02 20.76 18.3
52.9
31.8
87.8
77.6
ATB= 542.47
SB= Seasonal Biomass, TSB= Total Seasonal Biomass, SRB= Seasonal Relative Biomass, TB= Total Biomass, ATB= Annual Total Biomass, ARB= Annual Relative Biomass. W= Winter, S= Spring, Su= Summer, A= Autumn. Table 3. Component Weights in PCA Variables
Temperature Salinity Depth Substrate Biomass
Component 1
0.465 0.512 0.357 0.434 0.453
2 (83.5%) –0.472 –0.387 0.631 0.477 –0.031
and Laurencia pacifica (4.5%) (Table 2). The remaining species comprised 33% of the biomass. Principal components analysis The PCA detected two components that jointly account for 83.54% of the variability in the original data. According to eigenvectors, salinity was the most important variable in the first component while depth and temperature were the most important ones in the second component (Table 3). This analysis defined a close relationship between La Hielera (1) and El Dátil (2), as well as among Isla Brosa (3), Isla Piedra
212
Figure 4. Principal components analysis.
Norte (4) and Isla Piedra Sur (5). Campo Ejidatario (6) remained as an independent station (Fig. 4).
Discussion and conclusion The results show that several gradients are evident from the lagoon’s mouth to the head, namely temperature and salinity increased while depth and water movement decreased, and evaporation rates increased due to a high incidence of sun radiation. Tidal effects also influenced temperature and salinity, as observed in the lagoon’s inner portion where salinity rose from 42‰ to 47‰ during ebb tide. To note, depending of the position of the sampling stations in the lagoon are their environmental characteristics. The significant differences in average seasonal biomass (SAB) and total biomass (TB) throughout the year are related to: species richness, seasonal fluctuations in the biomass of some species, and variability of the environmental parameters. The highest SAB and TB numbers in the summer coincide with the maximum species richness; whereas the lowest SAB and TB in the spring coincide with the minimum species richness. Spyridia filamentosa, a tropical species, was observed when water temperature was high, and its biomass reached a peak during the summer. Polysiphonia pacifica also contributed to the increase in biomass in the summer, both contributing with only 25% of total biomass in this season. Other authors report the highest biomass of S. filamentosa during the summer in tropical and subtropical lagoons (Sánchez et al., 1989; Cruz et al., 1998; Núñez & Casas, 1998). Ectocarpus commensalis showed a preference for places with a hard substrate and also with the presence of seagrass (Zostera marina Linnaeus), which is its main substrate. The highest biomass for this algae
was observed in the summer, coinciding with a high seagrass abundance. McQuaid (1985) mentions that there is a close correlation between seaweed biomass and abiotic factors. To this respect, Graham & Wilcon (2000) point out that the main abiotic variables affecting intertidal seaweed biomass are temperature, light, wave force, salinity and nutrient concentration; temperature being amongst the most important ones. The seasonal variations detected in this study are in line with those obtained by Núñez & Casas (1998) for Laguna San Ignacio, Baja California Sur, Mexico, where biomass reached a maximum during the summer when water temperature was high, and decreased when temperature dropped. In addition, McQuaid (1985) found that the occurrence of optimal tidal conditions in the summer, when sun radiation and sea temperature were both high, resulted in particularly high biomass of the dominant seaweed species growing in a temperate costal area. Kornfeldt (1984) reported a marked seasonal variation in seaweed biomass in Kullen Sweden, with the highest biomass occurring in the summer when the temperature increases. As regards the spacial variation of biomass, a relationship between biomass and both species richness and water motion was detected in the different sampling stations. Isla Brosa (3) and Isla Piedra Norte (4) presented the highest SAB and species richness values, whereas La Hielera (1) and El Dátil (2) had the lowest SAB and species richness. In the first two stations water motion was moderate, while stations 1 and 2 showed a greater water disturbance. Cruz et al. (1998) mention a similar trend between biomass and species richness in some localities within a tropical bay. Molloy & Bolton (1995) reported that the decrease in the biomass of Gracilaria in Luderitz lagoon, Namibia, was caused by water disturbance, as most beds occurred in shallower water. Littler et al. (1985) found highest biomass of the filamentous group, that was the dominant in a sheltered site, was correlated with relatively low levels of physical disturbance and wave turbulence, contrasting with a site exposed to wave action. It is likely that the combination of a sandy substrate and a greater water disturbance in the sampling stations located at the lagoon’s mouth results in less stability, in turn reflected in lower specific richness and biomass. By contrast, stations located in the central portion of the lagoon, with a rocky substrate, show a moderate water motion while temperature and salinity vary to a lesser extent. For this reason, these stations are probably more stable and, consequently,
213 they support a higher species richness and biomass. For its part, the station at the head of the lagoon, with a sandy substrate but a low water motion, shows intermediate values for species richness and biomass. Trono & Saraya (1987) mention that the intensity of water movement and the availability of a solid substrate appeared to exert a significant control in the distribution of the dominant seaweeds. Temperature and salinity are important factors also influencing the spatial variation of macroalgal biomass (Virnstein & Carbonara, 1985). In this study, species with temperate affinities and a low tolerance for warm temperatures displayed a higher biomass near the mouth (La Hielera and El Dátil) where the temperature was at its lowest. In contrast, species with a tropical affinity, such as Hypnea valentiae and Dasya baillouviana, were more abundant at the head (Campo Ejidatario), where the highest temperatures were recorded (Abbott & Hollenberg, 1976; Alvárez & Granados, 1992). The conditions of hypersalinity restrain the presence of species with little tolerance to high salinities, whereas species richness increases in areas where salinity decreases (Britton & Morton, 1989). Each station showed a particular seasonal pattern influenced mainly by the species with the highest biomass, as mentioned by Nuñez & Casas (1998). Acrosiphonia saxatilis, Polysiphonia scopulorum, and Chondria dasyphylla were abundant at station 4 (Isla Piedra Norte) during the spring. This, plus the absence of seaweeds in all other locations, resulted in significant differences in average biomass among locations. Similarly, during the autumn the biomass of Chaetomorpha linum and Anotrichium tenue was high in Isla Piedra Norte and Campo Ejidatario, respectively, whereas seaweeds were absent in locations 1 and 2. The high average biomass in the summer, particularly at Isla Brosa (3) and Isla Piedra Norte (4), resulted from the high biomass of some species (Spyridia filamentosa and Polysiphonia pacifica) and the high species richness present there. The close relationship between La Hielera (1) and El Dátil (2), as detected by the principal components analysis, can be explained by similarities in substrate (sandy), low temperatures and salinity, as well as a low seaweed biomass. On the other hand, Isla Brosa (3), Isla Piedra Norte (4) and Isla Piedra Sur (5) share rocky substrates and similar temperatures and salinity. Campo Ejidatario (6) was considered an independent station because its characteristics differed from all
other stations, namely high temperatures, a very high salinity, low depth, and a sandy-muddy substrate. Although using other techniques, some autors have found that the relationship between sites is determined by the abundance of seaweeds and specific environmental variables. For example, in southern California Littler (1980) carried out a cluster analysis using macrophyte cover data, and found that those sites most strongly influenced by the cold California Current System formed a group broadly separated from sites exposed to predominantly warmer water. Cruz et al. (1998) used a cluster analysis to define phycofloristic associations within La Paz bay. They concluded that the variations in biomass, the type of substrate and the geographic proximity of locations determined these associations. Furthermore, León et al. (1993) mentioned that similarity increases when locations are geographically close. Potentially important species in Laguna Ojo de Liebre in terms of biomass, wide spatial and temporal distribution, and potential use were: Spyridia filamentosa, a source of antibiotics (Robles & Ballantine, 1999), Entheromorpha clathrata as human food and a source of pharmacologically active substances (Pacheco & Zertuche, 1996; Aguilera, 1999), Dasya baillouviana, also a source of antibiotics (Fenical & McConnell, 1976), Hypnea valentiae, a source of carragenan (Knutsen et al., 1995; Melo et al., 1997), and Sargassum sinicola, as human food and animal foodstuff, and a source of alginates and antibiotics (Casas & Sánchez, 1992; Marín, 1999).
Acknowledgements The Interdisciplinary Center of Marine Sciences (CICIMAR-IPN) and the National Council for Biodiversity (CONABIO) financially supported this survey. Authors are grateful to COFAA and EDI for its support, as well as to CONACyT, and PIFI for a grant provided to one of the authors. We appreciate the help of the Ichthyology and Macroalgae groups for their assistance during material collection activities.
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