Characterization of fish assemblages in a tropical coastal lagoon in the northwest Gulf of Mexico

Caracterización de los conjuntos de peces en una laguna costera tropical del noroeste del Golfo de México

Silvia Díaz-Ruiz¹, Marco Aurelio Pérez-Hernández² and Arturo Aguirre-León³

¹ Departamento de Hidrobiología Universidad Autónoma Metropolitana-Iztapalapa Apartado postal 55-535 Iztapalapa, CP 09340, D.F., México. E-mail: sdr@xanum.uam.mx

³ Departamento El Hombre y su Ambiente Universidad Autónoma Metropolitana-Xochimilco Apartado postal 23-181 Xochimilco, CP 0496, D.F., México.

Recibido en junio de 2002;
aceptado en septiembre de 2003.

Abstract

Tamiahua is one of the largest estuarine-lagoonal systems in the Mexican Gulf of Mexico. It has great economic and ecological importance due to high fisheries productivity and because it serves as a nursery, feeding and reproduction area for numerous populations of fishes and crustaceans. Spatial and temporal variations of fish diversity, abundance, dominant species and community inhabitants were determined based on samples taken on a bimonthly basis from May 1994 to March 1995. A total of 83 species, 62 genera and 32 families were collected, of which 14 species, 8 genera and 3 families were recorded for the first time in this area. Based on our collections and earlier reports, 136 species are known to use this lagoon system at some stage of their life cycle. The highest diversity and abundance values occurred during the rainy season (H'n = 2.7, D = 7.1, and J' = 0.6; biomass = 59.3 g m^-2, density = 5.8 ind m^-2, and average weight = 10.2 g ind^-1). Seasonal fluctuation of these parameters reflects the life cycles of different species (mainly the dominant species) related to the environmental dynamics of the ecosystem. Based on a graph-statistical analysis of the abundance and frequency data of 22,984 individuals, the fish species inhabiting the system were classified into four groups: resident, transient, irregular and rare. This analysis revealed the presence of 9 resident species, representing 77% and 73% of the total number of individuals and biomass, respectively. In order of importance, these species were Anchoa mitchilli, Membras vagrans, Hyporhamphus roberti, Bairdiella chrysoura, Eucinostomus melanopterus, Strongylura notata, Mugil curema, Achirus lineatus, and Cynoscion nebulosus.

Key words: fishes, ecology, diversity, abundance, Tamiahua, Gulf of Mexico.

Tamiahua es uno de los sistemas lagunares-estuarinos más extensos del Golfo de México. Es de gran importancia económica y ecológica debido a su alta productividad pesquera y constituye un área de crianza, alimentación y reproducción para numerosas poblaciones de peces y crustáceos. Las variaciones espaciales y temporales de la diversidad de peces, abundancia, especies dominantes y componentes comunitarios fueron determinadas de muestras tomadas bimestralmente entre mayo de 1994 y marzo de 1995. De un total de 83 especies, 62 géneros y 32 familias recolectadas, se registraron 14 especies, 8 géneros y 3 familias por primera vez en el área. Basados en esta recolección y trabajos previos, se conoce que 136 especies utilizan el sistema lagunar en alguna etapa de su ciclo de vida. Durante la época de lluvias se presentaron valores altos de diversidad y abundancia (H'n = 2.7, D = 7.1 y J' = 0.6; biomasa = 59.3 g m^-2, densidad = 5.8 ind m^-2 y peso promedio = 10.2 g ind^-1). Las fluctuaciones estacionales de estos parámetros reflejan los ciclos de vida de diferentes especies (principalmente las especies dominantes) relacionados con la dinámica ambiental del sistema. Con base en un análisis gráfico-estadístico utilizando datos de abundancia y frecuencia de 22,984 individuos, se clasificaron las especies que habitan en el sistema como residentes, en tránsito, irregulares y raras. Este análisis reveló la presencia de 9 especies residentes, representando 77% y 73% del número total de individuos y biomasa, respectivamente. En orden de importancia, estas especies fueron Anchoa mitchilli, Membras vagrans, Hyporhamphus roberti, Bairdiella chrysoura, Eucinostomus melanopterus, Strongylura notata, Mugil curema, Achirus lineatus y Cynoscion nebulosus.

Palabras clave: peces, ecología, diversidad, abundancia, Tamiahua, Golfo de México.

Introduction

Tropical lagoon-estuarine ecosystems are often characterized by high ecological complexity, high habitat and species diversity, and high productivity (Day et al., 1989). Because of these factors, the understanding of these ecosystems requires multi-disciplinary and integrative approaches to achieve sustainable management (Yáñez-Arancibia et al., 1992). Several fishery resources occur in the lagoon systems of the Gulf of Mexico, including a high diversity of important fish species. Despite their importance, the knowledge of fish ecology for many areas in the southern gulf is still incomplete, particularly with regard to distribution, abundance, feeding, growth and reproduction patterns. This information is very important for the development of rational fishery management plans (Yáñez-Arancibia et al., 1992). There is a great interaction between lagoonal habitat types and different fish groups because these areas are used during several stages of the life cycle of species with different biological requirements (Yáñez-Arancibia et al., 1985). Many of these species are currently exploited or constitute potential fishery resources. In addition, all of the species have some ecological importance.

Tamiahua is a large coastal lagoon on the northern coast of Veracruz in the western Gulf of Mexico. This is an area with rich biological resources, an important fishery, and a high degree of industrial activity. Hence, knowledge of the coastal ecosystems is necessary to foster enlightened management; however, ecological information for this system is scarce. Different aspects of the fish community structure in Tamiahua Lagoon have been studied (Reséndez, 1970; Kobelkowsky, 1991; Franco-López and Chávez-López, 1992), but these studies were mainly taxonomic in nature and did not consider ecological functioning. Considering the limitations of these studies, the economic importance of the fishery resources, and the potential for environmental impacts, we concluded that there was a need for a more detailed taxonomic analysis and a better ecological understanding of the fish community. Such an effort should be approached in an integrative and systematic way to obtain more complete information on the potential and actual resources of the region and develop better conservation and management alternatives for the fish communities of the coastal zone. Therefore, the objectives of this study were: (1) to determine the composition of the ichthyofauna of Tamiahua Lagoon, Veracruz; (2) to characterize spatial and temporal patterns of the diversity, distribution and abundance of the fish community; and (3) to determine the dominant species and define the fish assemblages of Tamiahua Lagoon.

Study area

Tamiahua Lagoon is located in the western part of the Gulf of Mexico (21°06'-22°05' N, 97°23'-97°46' W). It is the largest coastal lagoon in the state of Veracruz (Mexico), with a surface area of 880 km², and a maximum length and width of 100 and 25 km, respectively. The lagoon is shallow, with a mean depth of 2.5 m and a mean tide range of 0.20 m. It is connected to the sea via two tidal passes, Tampachiche Inlet to the north and Corazones Inlet to the south, and receives the discharge of several rivers: Laja, Cucharas, Carbajal, Tancochin, and Tampache (fig. 1). The climate is Aw2, tropical subhumid, with rains in summer (García, 1988). There are three climatic seasons: the dry season from March to May; the rainy season from June to October, characterized by conventional rains; and the winter storm ("Nortes") season from November to February (Castillo-Rivera and Kobelkowsky, 1993; De la Lanza et al., 1998). There are a number of different aquatic environments in the lagoon system, including brackish and low salinity mangrove swamps, seagrasses, areas of high sedimentation, oyster reefs, and a mesohaline to polyhaline central basin. More details about this lagoon can be found in the work of Contreras-Espinosa (1993).

Material and methods

Fishes were collected bimonthly at nine sampling stations in May, July, September and November 1994, and January and March 1995, during the three climatic seasons (fig. 1). Nekton were collected during daylight hours (07:00 to 15:00) from depths of 0.3 to 2.0 m, using a 60-m beach seine net with a mesh size of 1.9 cm in the bag and 1.5 cm in the wings. One catch was made at each sampling station, for a total of 54 collections. Samples were fixed in 10% formaldehyde and later preserved in 70% ethanol. Temperature, salinity, dissolved oxygen, and depth and transparency of the water column were measured during each collection (table 1), as described in Díaz-Ruiz et al. (2000). In the laboratory, fishes were identified, counted, weighed and measured. Diversity H'n (Shannon and Weaver, 1963), species richness D (Margalef, 1969), and evenness J' (Pielou, 1966) were calculated, as well as bio-mass (gwetweightm^-2), density (ind m^-2), and average weight of the community (gind^-1) (Díaz-Ruiz et al., 2000). The diversity, abundance and mean weight were compared between seasons using the total data of each (two months per season), using ANOVA with significance P < 0.05 (Daniel, 1997); in the presence of significant differences, Tukey's test (Zar, 1999) was used to determine in which season and parameters these differences occurred. The determination of fish assemblages was based on the graphical interpretation of the nonparametric association test of Olmstead and Tukey (Stell and Torrie, 1988; Sokal and Rohlf, 1997). Frequency and abundance of each species were related to the total number of sampling events (54 captures). A graph with four quadrants was obtained, each corresponding to one of the following groups of species: (A) transient, (B) resident, (C) irregular, and (D) rare. The partition of the y-axis originates in the median value of the average numerical abundance data (No. ind/capture), ordered in a progressive and upward way. The partition of the x-axis (frequency) settles down at the 50% level (Ibáñez-Aguirre and Solís-Weiss, 1986; Torres-Orozco and Zanatta, 1998). From this level, the degree of permanence of any species inside the sampled area could be considered resident species (Deegan and Thompson, 1985; Yáñez-Arancibia et al., 1985).

Results

Ichthyofaunal composition

We analyzed 22,984 individuals with a total weight of 174,368 g. A total of 83 fish species of 62 genera and 32 families were identified, of which 14 species, 8 genera and 3 families were recorded for the first time in the area (table 2).

Seasonal and spatial variation of diversity

Seasonal and spatial variation of abundance

The highest number of fishes, 9337 (40.6%), was captured during the rainy season, while 7734 individuals (33.6%) were caught during the dry season and 5913 (25.7%) during the Nortes season. The total biomass taken was 174,369 g, of which 94,894 g (54.4%) were obtained in the rainy season, and 42,975 g (24.6%) and 36,500 g (20.9%) in the dry and Nortes seasons, respectively. Biomass per unit area was higher in the rainy season, with 59.3 g m^-2, and lower during the Nortes, with 22.8 g m^-2. The highest value, 12.5 g m^-2, occurred at station 6 during the rainy season and the lowest, 0.30 g m^-2, at station 9 during the Nortes. According to ANOVA, significant differences were found for the biomass. The Tukey test showed that the differences were between the dry and rainy seasons, and between the rainy and Nortes seasons (P < 0.00113). Density showed a similar pattern, with the highest value, 5.84 ind m^-2, during the rainy season and the lowest, 3.7 ind m^-2, during the Nortes. The highest density, 1.5 ind m^-2, was recorded at station 2 in the rainy season and the lowest, 0.14 ind m^-2, at station 9 in the dry season (table 3, fig. 3). The average weight per fish showed a similar pattern to biomass and inverse to that of density. The highest average weight per fish, 10.2 g ind^-1, occurred in the rainy season, and the lowest value, 5.6 g ind^-1, in the dry season. Spatially, station 4 had the highest average weight, 18 g ind^-1, and station 8 the lowest one, 2.6 g ind^-1, both during the dry season (table 3, fig. 3). The statistical analysis did not show any significant differences among seasons for density and average weight (P > 0.2981).

Fish assemblages

Discussion

In this study, 83 species were identified, of which 14 were new records for the study area. The total number of species reported for Tamiahua Lagoon by other authors plus those identified in this study is 136, which represents 42.76% of the 318 species reported by Reséndez and Kobelkowsky (1991) for 13 lagoon systems of the Gulf of Mexico. For the study area, the works of Reséndez and Kobelkowsky (1991) and Franco-López and Chávez-López (1992) reported a combined list of 122 species. Based on the results for Tamiahua Lagoon, as well as elsewhere in the southern Gulf of Mexico, we believe that further effort in this lagoon would result in the capture of additional species, in terms of additional habitat type studied. These understudied areas include submerged vegetation patches, the intertidal margins of mangrove forests of the lagoon basin, and swamp zones and flood plains with freshwater influence. In this respect, Miller (1986) considers that the basins of the Pánuco and Tuxpam rivers and their tributaries (that bound the study area) are important centers of dispersion and endemism for the freshwater fish fauna. Many of these species have the capability to inhabit brackish waters and invade lagoon areas. Also, it is probable that species of marine affinity found in other lagoon systems of the southern gulf also inhabit Tamiahua Lagoon. We assume this because the Tampico-Cabo Rojo-Tuxpam coastal area (covering the entire Tamiahua basin) is regarded as a zoogeo-graphic transition zone of fish communities of the Carolinean (to the north, with temperate-warm components) and the Caribbean (to the south, with subtropical-tropical components) marine provinces (Castro-Aguirre et al., 1986). Tamiahua has the third highest number of fish species of the Mexican coast of the Gulf of Mexico, after Términos Lagoon, with 216 species (Reséndez and Kobelkowsky, 1991; Yáñez-Arancibia et al., 1988), and Tuxpam-Tampamachoco, with 179 species (Pérez-Hernández and Torres-Orozco, 2000).

Spatio-temporal variation in diversity and abundance

The lowest values for diversity and abundance were recorded during the Nortes season, with 56 species (table 3). During this time of the year, the different habitats of the system are used by a great number o species, including areas of seagrasses and mangrove systems, the inlets and adjacent continental shelf. Few abundant species were recorded during this time of the year. The average weight per individual of the populations was also small (6.2 g ind^-1) due to the decrease in numerical abundance during the Nortes season. The most abundant and frequent species during this season were Anchoa mitchilli, Ariopsis felis (Linnaeus, 1766), Baridiella chrysoura, Eucinostomus argenteus (Baird and Girard, 1855), Hyporhamphus roberti, and Membras vagrans. The behavior of these species has been observed in other tropical ecosystems by Díaz-Ruiz et al. (1982), Chavance et al. (1984), Aguirre-León and Yáñez-Arancibia (1986), Yáñez-Arancibia and Lara-Domínguez (1988), and Aguirre-Léon and Díaz-Ruiz (2000). Other species use the lagoon as a temporary feeding and protection area, such as Archosargus probatocephalus (Walbaum, 1792), Diapterus auratus, Harengula jaguana (Linnaeus, 1758), Lutjanus griseus (Günther, 1870), and Opsanus beta (Goode and Bean, 1882). The species Anchoa lyolepis (Evermann and March, 1902), Baridiella chrysoura, Eucinostomus gula (Quoy and Gaimard, 1824), Eugerres plumieri (Cuvier, 1830), Diapterus rhombeus (Cuvier, 1829), and Orthopristis chrysoptera (Linnaeus, 1766) use the system as an area of protection and/or maturation.

An increase in diversity and abundance (table 3) was observed during the rainy season, and bigger fish were recorded in the seagrass areas. This shows that the study area is used by many fish species that take advantage of the predominant environmental conditions at this time of the year, such as lower salinity, higher turbidity and increased primary production resulting from high river discharge in adjacent estuarine systems (Contreras-Espinosa, 1993). Similar processes have been observed in other coastal systems of the Gulf of Mexico (Deegan et al., 1986; Yáñez-Arancibia et al., 1988; Aguirre-León et al., 1998), such as Términos Lagoon, where the highest biomass, number of species and abundance of juveniles occur at the end of the rainy season. During the rainy season, mean weight (10.2 g ind^-1) increased in our study area due to the increase in the weight of the species, some of which spend all or great part of their life cycle in the estuarine-lagoonal area, like A. mitchilli, B. chrysoura, E. gula, H. roberti, M. vagrans and Mugil cephalus (Linnaeus, 1758). In addition, there was a significant increase in total fish biomass because a number of large marine or estuarine species used the lagoon for feeding and/or reproduction, such as Cathorops melanopus (Günther, 1864) (42.3 g ind^-1), Lagodon rhomboides (Linnaeus, 1766) (35.6 g ind^-1), Mugil curema (29.0 g ind^-1), Orthopristis chrysoptera (30.2 g ind^-1), and Strongylura notata (21.7 g ind^-1).

During the dry season, there were intermediate values of diversity and abundance (table 3), and salinity and transparency were high (table 1). Many juveniles and pre-adults (50-170 mm TL) migrate from the sea to the lagoon and use the area to feed and grow. This is evident because of the larger number of species with low average individual weight (5.6gind^-1) and abundance of small individuals, such as A. mitchilli and L. rhomboides. This behavior is mainly related to the environmental heterogeneity of the lagoon and to patterns of nekton migration for reproductive or feeding purposes (Huh and Kitting, 1985; Franco-López and Chávez-López, 1992). These strategies are closely related to the optimum use of the resources of the ecosystem and are reflected in the seasonal changes of diversity and abundance of the fish fauna, such as C. melanopus, E. gula, M. curema and O. chrysoptera (Hook, 1991; Díaz-Ruiz et al., 2000). In other coastal systems of the Gulf of Mexico, the relationship between the environmental behavior of the system and the life cycle of the species has been studied, which has been reflected in the variations of diversity and abundance of the fish community (Díaz-Ruiz et al. , 1982; Aguirre-Léon and Yáñez-Arancibia, 1986; Yáñez-Arancibia and Lara-Domínguez, 1988). Based on this, we conclude that this lagoon functions as an area of feeding, growth, reproduction, and/or protection for numerous species of fish.

The average values of the abundance parameters obtained for each group from the Olmstead and Tukey test indicate that the fish community was dominated by a few species, each with a great number of small-sized individuals. Thus, 11% of the species in the fish communities of the study area were residents (all dominant) and 89% were transients and irregulars. We therefore conclude that Tamiahua Lagoon is used mainly as a nursery area by a few species, and as area of refuge or temporary feeding by an intermediate number of species. The presence of a great number of irregular visitors, of low abundance and frequency but with higher weight per species, shows that many adult fish use the area in an irregular manner. The presence of few resident species, an intermediate number of transient visitors and many irregular visitors, has been described and discussed as characteristic of estuarine and lagoonal zones, where spatial and temporal habitat heterogeneity generates environmental changes to which only a small number of species are well adapted (Yáñez-Arancibia et al., 1985). These species develop abundant populations as a function of their high survival and fecundity (Huh and Kitting, 1985; Yáñez-Arancibia et al., 1993). Based on the adaptations of the species, the nine dominant species determined for this lagoon system can be grouped into different fish community types: A. mitchilli, B. chrysoura, M. curema, A. lineatus, and E. melanopterus behave as temporary estuarine inhabitants; M. vagrans, C. nebulosus, and S. notata are eury- haline marine species; and H. roberti is a marine stenohaline organism. Despite these differences, a common characteristic to all of them was that most of the population was represented by juvenile stages (Yáñez-Arancibia et al., 1985; Aguirre-León and Yáñez-Arancibia, 1986; Ayala-Pérez et al., 1995).

Most of the sampling stations (1, 2, 3, 6, 8) were located in the shallow margins of the lagoon (mean depth of about 0.80 m), where the submerged aquatic vegetation is dominated by Halodule wrightii Aschers (1868) and Ruppia maritima Linneo (1753). Because of the numerical abundance, the frequency of the dominant species and the preponderance of juvenile individuals, it is likely that the vegetated areas of the lagoon are crucial for the continuous recruitment of early life stages of the populations. This is particularly true for those species with an estuarine-dependent phase, as is the case of C. nebulosus, M. curema and S. notata (Yáñez-Arancibia et al., 1988). Several authors have shown that vegetated areas are important habitats for estuarine nekton populations, with specific areas associated with characteristic fish associations (Orth et al., 1984; Livingston, 1985; Lubbers et al., 1990). Vegetated areas have high food availability and support benthic populations which also serve as food for nekton. Finally, the vegetation provides juveniles with protection from predators. Characteristic fish communities have been described for several lagoon systems of the Gulf of Mexico and South Atlantic coast of North America (Ross and Epperly, 1985; Rozas and Odum, 1988; Yáñez-Arancibia et al., 1993), and the majority of the dominant species identified for Tamiahua Lagoon are also important in the fish associations of these coastal systems. Most of the nekton species in these systems have typical estuarine-dependent life cycles, with seasonal migrations coinciding with periods of high productivity and food availability (Yáñez-Arancibia et al., 1985, 1993). This temporal variability is also reflected in the diversity, abundance and biomass of the fish associations in Tamiahua Lagoon. Other ecological studies on the spatial and temporal patterns of the structure of fish communities in the southern Gulf of Mexico have demonstrated that important fishery species are determined, in terms of abundance, biomass and frequency, by the physical and structural features of these systems. These features include areas with submerged vegetation, the presence of extensive mangrove forests, climatic-meteorological conditions, fluvial discharge, hydrology, and tide range (Deegan et al., 1986; Hook, 1991; Aguirre-León et al., 1998).

Acknowledgements

We thank the Universidad Autónoma Metropolitana-Iztapalapa for institutional and financial support of this research. This study is part of the project Evaluación Geoquímica Ambiental y Diagnosis de la Zona Costera de Veracruz: Lagunas de Tamiahua, Pueblo Viejo y Tampamachoco, sponsored by CONACYT-3232-T9308/UAMI. We acknowledge the help of Oswaldo Pérez-Solís and Enrique Cano-Quiroga in processing some of the fish samples. We also thank John W. Day Jr. for his critical review of an early version of the manuscript, and the anonymous reviewers for their comments and suggestions.

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