Acta Biológica Colombiana

INTRODUCTION

Estuaries are highly productive aquatic ecosystems; the combination of marine water masses with variable freshwater flows contributes to the creation of valuable habitats for fauna and flora, including fish species with food and commercial value (Abrantes et al., 2015). The value of these habitats lies in the fact that they serve as nursery grounds for marine, freshwater, and estuarine fish species, providing them with different food sources and as protection sites against predators. Vegetation zones such as mangroves and submerged vegetation beds cover this ecological function, especially for estuarine- dependent fish species that predominate in estuarine assemblages, so changes in their composition provide valuable ecological information about the functioning of these ecosystems (Fodrie et al., 2009). Furthermore, it is assumed that environmental degradation of estuaries is directly reflected in changes in fish community structures, and it is recognized that these effects are difficult to determine because of the mobility between habitats and the migratory movements of estuarine- dependent species. However, it is also a fact that, over time, pollution processes affect the composition of fish species and the ecological processes in which they participate. Therefore, an advantage of determining changes in fish assemblages over time is that it allows for establishing working guidelines for understanding the influence of natural disturbances and anthropogenic impacts, supported by data sets obtained over broad spatial and time scales (Connell et al., 2008). Changes in ecological and feeding guilds can express different responses to disturbances; thus, these analyses allow monitoring the stability of fish communities as an indicator of changes in the health of an estuarine ecosystem (Sheaves et al., 2012). The Alvarado Lagoon System (ALS) is important in the coastal zone of Veracruz for its natural values as an ecosystem; it has been recognized as an area of importance for bird conservation (SEMARNAT, 2010) and for the West Indian manatee Trichechus manatus L. manatus, which is a threatened species (SEMARNAT, 2018). However, fish have not been integrated into these natural values. Therefore, this contribution updates the taxonomic information of fish species and analyzes the composition of the assemblages from 1966 to 2008 based on the comparison of composition, species richness, and estuarine use of ecological and trophic guilds.

MATERIALS AND METHODS

The Alvarado Lagoon System (ALS) is in the southeast of the state of Veracruz between 18°52′15″ N to 18°23′0″ N and 95°5′32″ W to 95°42′2″ W. It extends 26 km from Isla Vives to Camaronera Lagoon, covering an area of 6,200 ha. It is a fluvial- lagoon system formed by a central body connected to the lagoons of Buen Pais, Camaronera, and Taliixoyan; the Blanco, Acula, and Papaloapan rivers drain the system that communicates to the sea through an artificial channel in the Camaronera Lagoon and the natural communication of Boca de Alvarado.

The environmental characteristics of ALS are shown below. The discharge from Papaloapan River is 40 million m³ per day (De la Lanza 2017). The average depth is 2.5 m. The study area has Aw2(i) a climate and three climatic seasons: the dry season occurs from March to June, the average temperature is 32°C and prevailing warm and humid winds are S- SE; the rainy season occurs from July to October, with an average rainfall of 2,100 mm and tropical storms and hurricanes; the cold front season ("north winds") occurs from November to February, the temperature may drop to 18°C, prevailing boreal winds are N- NW and rainfall is low. Vegetation: mangrove; riverine forests occupy an area of 57,713 ha and the dominant species is the red mangrove Rhizophora mangle L. Aquatic vegetation: submerged, meadows of Ruppia maritima L., emergent species such as Typha domingensis Pers. and Cyperus articulates L. are present, and in the rainy season Eichhornia crassipes (Mart.) Solms upwells massively (Garcia, 2004; Moran- Silva et al., 2005).

The collection methods corresponded to the sampling methods reported for the fish collections in the ALS between 1966 and 2008, with respect to frequency, collection timing, and fishing gear. Resendez- Medina (1973) did not present information on the sampling frequency during 1966- 1968, but trawls, throw nets, gillnets, and hooks were used. Chavez- Lopez et al. (2005) sampled bimonthly from 1987- 1991, 2000- 2002, and 2003- 2004 with 0.25″ trawls. Franco- Lopez et al. (2018) sampled bimonthly from 2007- 2008 with 0.25″ trawls. The publications of Resendez- Medina (1973), Chavez- Lopez et al. (2005), and Franco- Lopez et al. (2018) were used to update the fish species list. The validity of taxa and scientific names was verified using reports of Fricke et al. (2022) and Froese and Pauly (2021). The nomenclature of species in the family Cichlidae was updated using reports by Kullander (2003), Schmitter- Soto (2007), McMahan et al. (2015), and Rican et al. (2016). Recently, Tavera et al. (2018) recovered the genus Rhonciscus Jordan et Evermann for the family Haemulidae, in addition to the revision of the genus Bairdella Gill by Marceniuk et al. (2019).

The information was divided into collection periods (CPs) with CP1 corresponding to 1966- 1968; the remaining CPs were defined in periods covering the three climatic seasons. Thus, CP2 to CP5 cover December 1987 to August 1991, CP6 and CP7 from June 2000 to June 2002, CP8 from April 2003 to July 2004, and CP9 from 2007 to 2008. The sampling sites are presented in (Fig. 1).

Figure 1.: Alvarado Lagoon System and sampling sites from 1966 to 2008

Species composition per CP was considered as an assemblage (Fauth et al., 1996). The ecological category of each species was defined using the criteria of Potter et al. (2015), adjusted for the ALS based on the frequency of occurrence and period of estuarine use by the species. The ecological categories were: Estuarine- dependent Marine (EM), Marine Opportunistic (MO), Estuarine Species (ES), and Freshwater Opportunistic (FO). The categories of species permanence in the estuary were defined by the frequency of occurrence of each species in the CPs: recurrent species (r), with frequencies in the CPs ranging from 60 to 100%; persistent species (p), which occurred in frequencies from 31 to 69%; and sporadic species (s) whose frequency is less than 30%. The trophic level of species was compiled using information available in FishBase (https://www.fishbase; Froese and Pauli, 2021). Level one is assigned to primary production sources and level two to herbivorous and detritivores consumers. The remaining levels are assigned by food combinations. Level three corresponds to heterotrophic consumer species of invertebrates, zooplankton, and benthic crustaceans. At level four, species consume fish only or in combinations with minor proportions of macrocrustaceans.

RESULTS

Based on the information compiled, the fish composition in ALS consists of 113 species, 82 genera, and 39 families. The list of species, ecological guild, and trophic guild by species is presented in Appendix 1; it is important to highlight that only Rhadmia guatemalensis Gunther 1864, is recognized as a threatened species (SEMARNAT, 2018). Species richness ranged from 43 in CP3 and from 55- 60 species in CP1 and CP4 to CP8 as well. In contrast, 45 species were collected in CP9 only during the mouths of the rivers flowed into the ALS.

The index of Species Richness (li) tended to increase from 1 to 2.52; in contrast, the index of Rarity (Qi) ranged from 0.2 to 0.3. The relationship between these indexes indicated that a greater influence of the recurrent and persistent species group on the composition of fish assemblages in the ALS occurred. The range of Qi values indicated the presence of low numbers of sporadic species per CP (Table 1).

Table 1.: Variation of species richness index (li), rarity index (Qi) in fish assemblages of the ALS between 1966 and 2008.

Similarities in species composition were highest among CP2, CP4, and CP5 (0.73 - 0.86); in this group, CP3 was separated. Another group was formed with CP6, CP7, and CP8 (0.82 - 0.78). The least similar assemblages were CP9 (with similarity of 0.64) and CP1(0.48); NMDS analysis reiterated this group formation (Stress = 0.05; Fig. 2).

The comparison of species richness by ecological guild shows that estuarine- dependent marine species were the most numerous in the assemblages, contributing percentages of 40 to 55% per CP. In this guild, the families Gerreidae, Sciaenidae, Mugilidae, and Belonidae stood out. In contrast, the most notable numerical variations occurred in the guild of sporadic marine species, mainly from marine families such as Carangidae, Sciaenidae, Clupeidae, Lutjanidae, Haemulidae, and Sparidae, which were recorded more in CP1, CP2, and CP5. The freshwater species guild also showed changes in specific richness related to variations in the marine guilds, e.g., between CP6 to CP8 the number of freshwater species mainly from the family Cichlidae increased, while marine species decreased. Comparison of species composition by ecological guild by assemblage showed no significant differences (H = 0.944, p > 0.05) (Table 2).

Figure 2.: NMDS analysis chart showing the clustering of collection periods (CPs) according to most fish assemblage similarities. The species composition similarity was highest among CP2, CP4, CP5 and CP3 (0.73 - 0.86). For CP6, CP7, and CP8 similarity was 0.78-0.82. The least similar assemblages were CP9 (0.64) and CP1 (0.48).

During the period analyzed, the ALS fish community was composed of 35 recurrent species, both marine species such as Diapterus auratus Ranzani 1842, Diapterus rhombeus Cuvier 1829, Achirus lineatus L. 1758, Anchoa mitchilli Valenciennes 1848, Ariopsis felis L. 1766, and Hypanus sabinus Lesueur 1824, and freshwater species such as Mayahoros urophthalmus Gunther 1862, the introduced tilapias Oreochromis aureus Steindachner 1864, Oreochromis niloticus L. 1758, and Poecilia mexicana Steindachner 1863, as well as estuarine species of the family Gobiidae such as Gobiionellus oceanicus Pallas 1770, three catadromous species of the genus Centropomus Lacepede and Lutjanus griseus L. 1778, which is considered to be a mainly marine species, among others. In the persistent species group, marine species such as Hemiramphus brasiliensis L. 1758, one catadromous species Centropomus ensiferus Poey 1860, seven species of the families Gobiidae and Eleotridae, as well as seven freshwater species such as Trichromis salvini Gunther 1862, Vieja synspila Hubbs 1935, Belonesox belizanus Kner 1860, Dorosoma spp. and Rhamdia guatemalensis, were found. The group of sporadic species corresponded mainly to marine species of the families Carangidae, Lutjanidae, Sparidae, Clupeidae, and Sciaenidae. In the composition of the trophic guilds, microinvertebrate, macrocrustacean, and fish consumers predominated in all CPs, with no statistical differences (H = 2.077, p > 0.05; Table 3).

Table 2.: Variation in species richness of ecological guilds in ALS from 1966 to 2008. The Comparison of species richness of ecological guilds by assemblage showed no significant differences (H = 0.944, p > 0.05). Abbreviations from appendix 1. Abbreviations: EG: ecological guilds, ME: marine estuarine dependent, MO: marine opportunistic, FO: freshwater opportunistic, ES: estuarine species, CS: catadromous species. Occurrence category (O): r: recurrent, p: persistent, s: sporadic.

Table 3.: Number of fish species by trophic level of the ALS fish species assemblages, without statistical differences (H = 2.077, p > 0.05).

DISCUSSION

The fish species richness of the ALS places it among the most biodiverse estuaries in the Gulf of Mexico, with the caveat that there are few publications on estuarine fish biodiversity for this region (Chavez- Lopez and Rocha- Ramirez, 2020). The ecological composition of the ALS assemblages was dominated by estuarine- dependent marine species, a common feature in estuaries worldwide (Vasconcelos et al., 2015), and together with other freshwater and estuarine species, they form a group of 66 species of common occurrence in the ALS during the period studied. Different studies indicate that sporadically occurring species influence the temporal composition of the assemblages. In the ALS the numbers of these species were low and did not show up in the values of the species richness and rarity indices. However, different studies show that the community composition of estuarine fish over long time periods is strongly influenced by the presence of visiting marine species that are opportunistic and depend on the inter- annual variation of important environmental factors that favor them, such as salinity (Passos et al., 2013; Gonzalez- Sansón et al., 2018). Another notable difference between the fish assemblages of the ALS is the participation of the freshwater guild. For example, in CP6 the richness of opportunistic marine species decreased, but more freshwater species were recorded, such as Astyanax fascatus Cuvier, 1819, Belonesox belizanus, Rhamdia guatemalensis, Trichromis salvini and Thorichtyhs helleri Steindachner 1864, and the introduced tilapia Oreochromis aureus and O. niloticus. This evidence contrasts with that reported by Whitfield (2015), who states that freshwater species have physiological limitations for occupying estuaries. García- Seoane et al. (2016) points out that when salinity increases there is also an increase in the number of species of both estuarine- dependent and occasional marine guilds, with the total absence of freshwater species. Although it is recognized that salinity is the environmental factor that exerts the greatest influence on the composition of estuarine fish communities, in the ALS salinity does not seem to have this influence. For example, Villalobos- Figueroa et al. (1975) report that in the 1960s, river discharge determined the hydrological and salinity patterns of the lagoon system. In 1982, a channel was opened in the Camaronera Lagoon to increase salinity and promote shrimp production. Rosales- Hoz et al. (1986) recorded a substantial change from 4% before the opening to 25% during its operation; however, these events did not produce an effect on the composition of fish assemblages. De la Lanza (2017) noted that an oligohaline- mesohaline salinity pattern has been constant over the last 50 years, which explains the guild combination of the recurrent species group in ALS. This evidence indicates that the fish community in the ALS has been composed of assemblages formed by constant and stable marine and freshwater fish species reflecting the hydrological conditions prevailing during the time span analyzed. Changes in the taxonomic composition of estuarine fish assemblages have been shown to be a sensitive indicator of environmental modifications caused by alteration and degradation of habitats or water quality (Villeger et al., 2010). When these events occur in estuaries, fish assemblages are unstable and show a highly variable species composition over time (Scyphers et al., 2015), severe declines in species richness (Cardoso et al., 2011) and modification of the energetic pathways of the trophic web due to altered food sources (Baptista et al., 2015). In regard to the trophic guilds of ALS, the higher frequency of invertebrate, macroinvertebrate, and fish consumers supports the constancy of the fish community in recent decades; this fact also indicates that the species of the recurrent group of ALS are examples of life histories that have allowed them to tolerate the variations of the estuarine system over time.

CONCLUSIONS

In the ALS, 113 fish species were recognized. The ecological guild of marine species with estuarine dependence was the most numerous; the presence of species of freshwater origin was also notable. The results obtained highlight the importance of the group of 66 recurrent, persistent, marine, and freshwater species that characterized the assemblages and contributed to maintaining the species composition of the community.

This information should not be taken as a guarantee of the environmental health of the ALS, but it can be a basis for proposing guidelines for future research. For example, the effects of human activities on the watershed or on the loss of aquatic vegetation habitats have not yet been assessed, nor have assessments of the potential effects of climate change on the biota of this ecosystem been initiated.