Background

México is a country with high biodiversity. It is also characterized by a high number of coastal lagoons and estuaries, which are used by its diverse fish communities, especially the ones associated to soft bottoms, a characteristic feature of this type of lagoons. Moreover, these lagoons play a major role in the reproductive cycles of many marine species, and are also used for commercial fishing (Galván-Piña et al., 2003).

Coastal lagoons are physically unstable areas characterized by spatial and temporal variations of water temperature, salinity, dissolved oxygen and turbidity (Palomino et al., 1996). This environmental complexity alongside low predation rates, favours their icthyofauna, which is characterized by juvenile fish that used these lagoons as feeding and breeding grounds. However, only few species that used these lagoons during the entirety of their life cycle, while others just use them during a specific part of their life cycle (Barjau-González, 2003).

There are many studies about the structure and dynamic of fish communities. For example, Olaya et al. (2008) compared the fish community assemblage of Santa Marta and Parque Natural Nacional Tayrona (PNNT) in Colombia. Méndez et al. (2008) compared fish diversity during daytime and nighttime between populations from Golfo Cariaco, Estado Sucre in Venezuela, because different species use the reef at different times according to their diurnal and nocturnal behaviour.

México has more than 100 coastal systems (coastal lagoons and estuaries), and 22 of these are found in the Baja California península (Lankford, 1977). The coastal lagoon of La Paz is characterized by its bathymetry, physicochemical variables, predominant sandy substrate on the north, and a combination of mud and sand on the south (Cervantes Duarte et al., 2001). Because of its particular environmental and physical features and because it has been the object of anthropogenic impact through the discharge of wastewater from the city of La Paz. The aim of the present study was to determine the taxonomic distinctness of the soft-bottom fish community of the coastal lagoon in the city of La Paz, Baja California Sur (BCS) in México.

1 Materials and Methods

1.1 Study area

The coastal lagoon of La Paz (Figure 1) is located south of La Paz Bay, in the state of Baja California Sur, between the parallels 24°11 and 24°06', and between meridians 110°19' and 110°25'. It is separated from La Paz Bay by an 11-km sand barrier known as “El Mogote” (Cervantes Duarte and Guerrero Godínez, 1987).

Six bi-monthly samplings were carried out in seven localities from August 2016 to June 2017 performing a total of 42 replicates (Table 1). An experimental trawl net with a length of 9 m, a vertical opening of 4.5 m, a mesh size of 1.5 inches, and metal doors of 95x50 cm, was used to catch the fish. The trawl speed was 3.5 km/h, sweeps lasted for 20 minutes at an average depth of 5 m at each locality. Sweeps in which no capture was recorded were considered as water sweeps, represented by zero. A 22 feet boat with a 75 HP four stroke outboard motor was used as a trawler. Physicochemical variables such as water temperature (°C) and salinity (UPS) were recorded at each locality using a YSI 2030 Pro multiparameter instrument.

All samples were processed in the fish ecology laboratory of the Autonomous University of Baja California Sur. Length of fish specimens was calculated using an ictiometer. Weight was determined using a digital scale Ohaus Explorer Pro. Species identifications were carried out using specialized literature. Ecological indices were analysed using the software PRIMER-E 6 & PERMANOVA+ version 1.0.2 and statistical analysis were performed using STATISTICA v 8.

The following taxonomic diversity analysis methods were used:

Fisher’s alpha diversity (α-Fisher) (Fisher et al., 1943): It is not commonly used but it is biologically well supported given that evaluates diversity more efficiently considering number of organisms and number of species (Condit et al., 1996). This parametric index assumes that species abundance follows a logistic distribution. Diversity analysis using this index are considered more accurate given that Shannon’s and Simpson’s indices depend on the number of the most common species (Medianero et al., 2003), therefore masking the importance of the rare species.

Taxonomic distinctness (TD Δ*) (Clarke and Warwick, 1999): This index evaluates taxonomic distance and species richness, using the total species abundance. This index has been considered a more precise measure of biodiversity, since it incorporates qualitative as well as quantitative aspects of the fauna or flora.

Average taxonomic distinctness (AvTD Δ+) (Clarke and Warwick, 2001): This index evaluates richness as well as the taxonomic distance of each species pair, defined through a Linnaean classification tree.

In both indices, each hierarchical taxonomic level gets a discrete and proportional value in a scale that goes from 0 to 100. These indices are independent of sample size and do not need data normality. For the first index, we used the total abundance data, standardized according to Clarke and Warwick (2001); for the second index, we used presence/absence data. To calculate these indices six hierarchical levels were used: species, genus, family, order, class and phylum.

2 Results

2.1 Environmental variables

Temperature between sampling sites was not significantly different (p=0.9675). Lowest temperature (23.28°C) was recorded at site five, whilst the highest was recorded at site one (25.42°C). However, temporal comparison showed significant differences (p=<0.05) between months, with the highest temperature recorded in August (28.17°C), whilst the lowest was recorded in February (21.43°C) (Table 2).

Salinity did not show significant differences (p=>0.05) between sampling sites. Lowest salinity was recorded at site one (31.78 UPS), whilst the highest was recorded at site four (33.68 UPS). Moreover, a comparison between months did not show sifnificant differences (p=>0.05), but the lowest value was recorded in April (31.90 UPS), whilst the highest value was recorded in October (33.97 UPS) (Table 2).

2.2 Taxonomic distinctness

A total of 2,763 organisms were collected from 42 samplings, belonging to the following families: Haemulidae (13), Sciaenidae (10), Gerreidae (8), Urotrygonidae (5), Paralichtyidae (4) and Serranidae (4). The five families with the highest number of genera were: Sciaenidae (9), Haemulidae (6), Gerreidae (4), Paralichtyidae (4) and Serranidae (3).

Fisher’s alpha diversity (α-Fisher), temporal and spatial analysis of this index did not show significant differences (>p=0.05). Highest value of this index was recorded in June (S= 21.83), and the lowest was recorded in February (S=10.66). Spatial comparison showed the highest value in site five (S=25.16), whilst the lowest value was recorded in site six (S=9.50) (Table 2).

Regarding Taxonomic Distinctness (TD ∆*) between sites, it was highest at site seven (65.01 units), whilst lowest was at site six (54.30 units). All sampling sites are located above or very close to the average in the tunnel (Figure 2). TD ∆* between months was highest in June (62.76 units) and the lowest was recorded in December (50.85 units) (Figure 3).

Average taxonomic distinctness (AvTD Δ+) between sites was highest at site six (66.19 units) and the lowest was at site three (58.21 units) (Figure 4). AvTD Δ+ between months was highest in April (64.53 units), and the lowest in December (55.86 units) (Figure 5).

3 Discussion

3.1 Environmental variables

According to temperature analysis of the coastal lagoon of La Paz, there were no significant differences between sites. When comparing to similar lagoons such as San Ignacio lagoon (Muñoz-Félix et al., 2017), located on the west coast of the state of BCS, authors reported no significant differences in temperature between sites (p=0.9736). Although San Ignacio lagoon is larger and deeper that our study site, temperature shows a similar pattern throughout both lagoons. Temperature analysis between months showed significant differences, similar to what was recorded in San Ignacio lagoon (Kosegarten-Villarreal et al., 2016; Muñoz-Félix et al., 2017). They reported similar temperatures, coldest month was December and warmest month was August, with a natural variation of temperature throughout the study, similar to what it is reported in the present study.

Salinity between sites did not show significant differences (p=0.5566). Previous studies in San Ignacio lagoon (Juaristi-Videgaray et al., 2014; Kosegarten-Villarreal et al., 2016; Muñoz-Félix et al., 2017) found significant differences between sites, probably because San Ignacio lagoon is directly connected to the Pacific Ocean, and its salinity changes from the mouth or outter part towards its inside, and because it is considered a hypersaline lagoon, high values were recorded (38.6 UPS). The coastal lagoon of La Paz is smaller and less deep than San Ignacio lagoon, it is not directly connected to the Gulf of California, it is first connected to La Paz Bay, which suggests that it is not subjected to great variation in its salinity. Barjau-González et al. (2014) reported the highest temperature in La Paz Bay during their period of study was recorded during August 2002 (29.63°C), whilst the lowest was recorded during March 2003 (22.41°C). They identified two climatic seasons in this area, warm and cold. Previous studies in San Ignacio lagoon (Barjau-González et al., 2015; Kosegarten-Villarreal et al., 2016; Muñoz-Félix et al., 2017) reported different salinity values, with the lowest recorded in April (31.5 UPS), and the highest recorded in June (38 UPS). The lowest salinity reported for San Ignacio lagoon is similar to what is reported in the present study for the coastal lagoon of La Paz, however, the highest salinity was different probably due to the oceanographic behaviour of San Ignacio lagoon, because the water exchange of this lagoon takes from three to four months, while the water exchange of the lagoon of La Paz takes less time (two to three months - L. Álvarez-Santamaría, personal communication, June 2017). Temperature and salinity records in the present study are similar to values reported by Allen and Horn (1975), Amezcua-Linares (1977) and Allen (1982), and they conclude that environmental variables like temperature and salinity are have an effect on fish diversity of coastal ecosystems.

Previous studies in coastal lagoons, bays, islands and seamounts, using visual census and fishing arts such as trawling net, have reported that fish diversity on the southern region of the Gulf of California, is influenced by water temperature, salinity, habitat, depth, currents, upwellings, gyres and surrounding flora and fauna (Rodríguez-Romero et al., 1994; 1998; 2005; Amador-Buenrostro et al., 2003; Galván-Piña et al., 2003; Muhlia-Melo et al., 2003; Barjau-González et al., 2012; 2014; 2015; 2016; Muñoz-Félix et al., 2017).

3.2 Taxonomic distinctness

Fisher’s alpha diversity (α-Fisher) is not commonly used to analyse diversity, however, it is biologically well supported because is not depending on sample size and evaluates diversity more efficiently considering number of organisms and number of species (Condit et al., 1996; Moreno, 2001; Magurran, 2004). We decided to use this index because the present data includes species with high and low abundance values, and using indices like Shannon (H’) and Simpson (S) depend on number of organisms of common species, therefore masking the importance of rare species. Spatial analysis of α-Fisher showed the highest value at site five (S=25.16), whilst the lowest value was recorded at site six (S=9.50) (Table 2). Comparing our results with other studies, Juaristi-Videgaray et al. (2014) carried out 11 samplings throughout San Ignacio lagoon, reporting that site seven (known as Cantil Cristal) had the highest α-Fisher (S=10.01), whilst site one (Canal del Cardón) had the lowest (S=0.83). The site Cantil Cristal is located on the inside of the San Ignacio lagoon, with a mixed substrate (sea shells, sandstone), whilst Canal del Cardón is located on the mouth of the lagoon, with sand as a substrate. Difference on the type of substrate might be the reason for different fish diversity in that area. These results are different to what we found in the lagoon of La Paz, probably due to a lower number of samplings and lower depth during sweepings than what is reported in the present study.

Temporal α-Fisher showed values above 10 units, higher than other study areas. Juaristi-Videgaray et al. (2014) reported that spring and summer had the highest values (S=12.15), whilst winter had the lowest (S=7.51). Barjau- González et al. (2016) reported a high α-Fisher during March (S=10.01), whilst October had the lowest value (S=7.87). Muñoz-Félix et al. (2017) reported the highest α-Fisher during August (S=10.19), and the lowest during December (S=1.08). Comparing these studies with our results, Fisher’s alpha diversity was higher than the one recorded for San Ignacio lagoon, probably due to higher exploitation compared to the lagoon of La Paz.

Taxonomic distinctness (Δ*) is an index that measures pure taxonomic relatedness. Clarke and Warwick (1998) established the use of this index to infer if an ecosystem can be considered anthropogenically impacted or in pristine conditions. Values are adjusted depending on the number of hierarchy levels used, six levels were used for the present study. The use of this type of ecological indices in México is relatively recent. Juaristi-Videgaray et al. (2014) reported spatial ∆* in San Ignacio lagoon with values from 49.95 to 66.67 units. Barjau-Gonzalez et al. (2012) reported spatial ∆* in San José island (study area close to the lagoon of La Paz) with values from 51.58 to 53.58 units. Barjau-González et al. (2014; 2016) reported spatial ∆* from eight sites of La Paz Bay, with values from 53.58 to 59.29 units. Spatial ∆* values in the present study (Figure 2; Table 2) are similar to those reported by Juaristi-Videgaray (2014), considering they only carried out four samplings and used a similar fishing art, whilst other studies used visual census. When just presence/absence data are considered for analysis, taxonomic diversity (Δ) and taxonomic distinctness (Δ*) converge in the same index, average taxonomic distinctness (Δ+), which is the length of taxonomic relatedness between two random species (Sohier Charlotte, 2008). Spatial and temporal Δ+ showed values close to the mean (Figure 3; Figure 4; Table 2). These results are similar to those reported in San Ignacio lagoon by Juaristi-Videgaray et al. (2014), in San José island by Barjau-Gonzalez et al. (2012), and in La Paz Bay by Barjau-González et al. (2014; 2016), with values close to the mean, and in some cases, closer to the confidence intervals. Our results are also close to the mean and between the confidence intervals. Because of similar values of Δ+ in those study areas, we infer that the lagoon of La Paz is in good condition.

Temporal and spatial taxonomic distinctness (Δ*) showed similar values, from 58.21 to 66.29 units (Figure 4; Table 2). These results are similar to previous studies, which suggests that from an ecological point of view, the lagoon of La Paz is healthy, compared to other study areas. Regarding temporal Δ*, its values are located close to the average (Figure 5; Table 2), and only the month of December locates outside the lower confidence interval. This is probably due to water sweeps, therefore, there were no catches in some of the sites, and because this index relies on presence/absence data, December had the lowest Δ* with 55.86 units.

4 Conclusion

Considering the anthropogenic activity that for many years affected the lagoon of La Paz through the discharge of wastewater from the city of La Paz, results from the present study suggest that fish taxonomic diversity is in equilibrium, based on phylogenetic relatedness of species, genera and families, and trophic ecology, represented by all 73 species. Because of the anthropogenic activities carried out for decades, fishers and inhabitants of the city of La Paz, are not fishing in this area, therefore allowing for a high diversity.

Authors' contributions

EBG designed and carried out fish collection, analysed data and wrote the manuscript. AKRP revised the manuscript. JMLV revised the manuscript. JAAQ georeferenced the sampling sites. All authors read and approved the final manuscript. Likewise, they declare no conflict of interest.

Acknowledgments

Authors would like to acknowledge the Departamento Académico de Ciencias Marinas y Costeras for funding the project in which this study took part. Autonomous University of Baja California Sur (UABCS) for allowing the use of its facilities (Laboratorio de Ecología de Peces). MSc Myrna Barjau Pérez Milicua for the english editing of the manuscript.

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