Record of three non-native fish species from the Alvarado Lagoon, Veracruz, Mexico

The proliferation of non-native species in the freshwater ecosystems of East Central Mexico is considered a primary threat to the integrity of local native community structure. However, a general understanding of consistent and predictable impacts of non-native species on native freshwater diversity is limited, in part, because of a lack of broad-scale studies including data from numerous localities across multiple drainages. In this study, we captured 85 neotropical fish belonging to nine species in the Alvarado Lagoon, Veracruz, southeast from the Gulf of Mexico. Of these, the presence of three non-native species was confirmed: the pantano cichlid Cincelichthys pearsei , the jaguar cichlid Parachromis managuensis and the vermiculated sailfin catfish Pterygoplichthys disjunctivus . The species settlement in the region is a consequence of aquaculture practices with food purpose and ornamental production


Introduction
The term "non-native species" refers to an infra or supraspecific species, subspecies or taxa introduced outside their natural distribution and with an increased distribution outside their natural range, including any part, gamete or propagule of such species (CBD 2009). These species are further classified as: translocated (introductions within the country from another river basin or freshwater ecoregion within a country) and exotic (introductions from another country, or continents) (Vitule et al. 2019). Based on this concept all of the native species of Mexico, that have been translocated to an area or region different from their natural or original one, are called non-native species (Medellín-Legorreta 2014). The capacity of survival, the rate of reproduction and the ease of establishment in the new habitat of non-native species represents a threat to native biodiversity, affecting public health and local economy (CBD 2009;DOF 2010). The effect of biological invasions by aquatic species has been widely documented, but the valorization of the effect is still inconclusive (Mendoza-Alfaro and Koleff-Osorio 2014). Still, there is a crescent necessity to attend to invasive species to avoid further damage and reduce the problems caused (Koleff 2017). The previous has led to the development of several preventive actions, risk analysis studies and the emergence of regulatory frameworks for the correct evaluation of the potential risks derived from the introduction of exotic aquatic organisms into a new environment (Mendoza-Alfaro et al. 2011).
In Mexico, many of the freshwater fish species have been introduced as a result of human activities. These intrusions generally cause negative effects such as the alteration of the trophic relationships in the recipient system (Martin et al. 2019), causing important long-term changes in the characteristics and dynamic of the aquatic systems (Díaz-Pardo et al. 2016). Currently, 104 species of exotic fish have been recorded in Mexico (Espinosa-Pérez and Ramírez 2015). Their introductions in combination with anthropogenic factors, such as the negligent management of aquatic ecosystems, have diminished native species populations and placed around 248 native species in the risk category (IUCN 2019). Thereupon, it is vital to keep the track of new non-native species introductions in the epicontinental ecosystems of the country. The aim of this paper is to contribute to this effort by confirming the presence of three exotic species in Alvarado Lagoon, Veracruz State, Mexico.

Materials and methods
The Alvarado Lagoon is located on the coast of central Veracruz State (Figure 1). It forms part of the Alvarado Lagoon System, which consists of four interconnected brackish, shallow coastal lagoons: Alvarado, Buen País, Camaronera and Tlalixcoyan, belonging to the hydrological region of the Papaloapan River Basin, located between the geographical coordinates 18°44′00″-18°52′15″N; 95°44′00″-95°57′00″W (Flores-Coto and Méndez-Vargas 1982;Ruiz-Fernández et al. 2014). During July 2019, fish collections were made at five points near Las Aneas locality (18°46′24.8″N; 95°46′40.9″W), one point per day, near the eastern edges of the Alvarado Lagoon. Fish were captured using two gillnets (lenght of 100 m, height of 2.5 m and mesh opening of 12.5 cm), which opereted parallel to the coast for a period of six hours during the first hours of the day. The catch was recovered by monitoring the fishing net every two hours. Species that have not been reported in previous faunal inventories were fixed in formaldehyde (10%), preserved in ethyl alcohol (70%) and deposited in the Colección Ictiológica of the Facultad de Estudios Superiores Iztacala (CIFI), UNAM (Sabaj 2019). Basic morphometric and meristic data were obtained ( Table 1). The taxonomic identity of each species was corroborated with the help of specialized taxonomic keys (Bussing 1998;Armbruster and Page 2006;Miller et al. 2009). All the research pertaining to this article did not require any registration consent.
The natural distribution of C. pearsei is in the Grijalva-Usumacinta region, in southern Mexico and northern Guatemala (Miller et al. 2009). Authorization for commercial fishing in different reservoirs in Mexico has promoted its farming and propagation, as is the case for the Dr. Belisario Domínguez "La Angostura" and Netzahualcóyotl "Malpaso" dams in Chiapas, Mexico. The species was firstly introduced to the dam "Miguel Alemán" in the middle part of the Papaloapan River. In 1968, the Tropical  planted there (Almeyda-Artigas 1991; SAGARPA 2016). Apparently, C. pearsei began to colonize and spread to the middle part of the Papaloapan River basin and in time it reached also the lower parts. Franco-López et al. (2018) conducted a study on the seasonal composition of three rivers that flow into the Alvarado Lagoon, of which C. pearsei is present in the Acula and Blanco rivers. Parachromis managuenesis (also guapote Jaguar or guapote Tiger) is a species native to Central America with natural distribution ranging from Honduras in the Ulúa River down to the Matina River in Costa Rica (Bussing 1998). Its introduction into different aquatic systems in southwestern Mexico is a consequence of the utilization of the species as food source and also its importance in the aquarium industry (Miller et al. 2009 (Kifune et al. 2004;Salgado-Maldonado 2006). Non-native populations of P. managuensis have been also established in the Grijalva-Usumacinta basin, in the Palizada lagoon system, in Términos Lagoon and Silvituc Lagoon in Campeche, Mexico (Vidal-Martínez et al. 2002;Mendoza-Carranza et al. 2018). Currently there is no evidence of its presence in the other parts of Papaloapan River basin or indications of how it reached the Alvarado Lagoon system. The closest records to the state of Veracruz are in Tabasco (Amador-del-Ángel and Wakida-Kusunoki 2014). Thus, the present study represents the first formal record of its occurrence in the Papaloapan basin and in the state of Veracruz, Mexico.
The natural distribution of Pterygoplichthys disjunctivus and its congeners in lagoon and riparian systems is wide in terms of the Amazon basin (Armbruster and Page 2006). This wide distribution is attributed to its high biotic potential as it is an ovoviviparous species with parental care, a vascularized stomach that helps with the task of efficient breathing and a body covered by thick modified scales to prevent predation (Hoover et al. 2004;Mendoza et al. 2007). In Mexico, the records of invasion of suckermouth armored catfishes, locally known as Devil fish (Pterygoplichthys anisitsi, P. disjunctivus, P. multiradiatus and P. pardalis), are well documented in comparison with other fish species, highlighting those records in states with a slope in the Gulf of Mexico: Campeche, Chiapas and Tabasco For Veracruz, the first records of the genus Pterygoplichthys were taken from the Chacalapa micro-basin that belongs to the Coatzacoalcos River basin. Subsequently, other records in the Interdunaria Lagoons appeared, corroborating its occurrence in the central and southern part of the state (Wakida-Kusunoki et al. 2016). It is probable that the route of introduction of P. disjunctivus into the Alvarado Lagoon has been related to fish leakage from aquaculture facilities or natural dispersion. Natural dispersion could have been caused by floods occurring during the rainy season in the terrestrial and riverine environments, between the Coatzacoalcos and Papaloapan. An evidence of such dispersion between these two basins comes from results of Wakida-Kusunoki et al. (2016), who detected presence of the Amazon sailfin catfish P. pardalis in two bordering localities (Hueyapan River of Papaloapan River basin and Comejen River of Coatzacoalcos River basin) with less than 7 km between them.
There is high probability that the three species will establish in the Alvarado Lagoon. Parachromis managuenesis has a high ability to establish populations in a wide range of lotic and lentic environments due to particular survival strategies, such as its ability to survive in hypoxic waters, toleration to high water temperatures, and bi-parental care (França et al. 2017). In addition, cichlids have a high degree of euryhalinity and are capable to survive in mesohaline conditions for long periods and could potentially use the brackish waters of Alvarado Lagoon System as vector for the dispersal to other environments (Welcomme 1988;Gutierre et al. 2014).
Possible establishment of the P. disjunctivus is especially worrying since it has been shown that this species displaces native species as a result of incidental ingestion of their eggs, competition, disruption of trophic dynamics, disease and parasite transfer. These effects may reduce the size of native fish populations and cause death of birds and damage of manatees populations (Mendoza et al. 2007). This species also causes resuspension of the sediment by excavating galleries of up to one and a half meters to nest, causing erosion and increasing turbidity. Devastation of one of the most important fisheries in Latin America in the 1960s at the Infiernillo dam in Michoacán can serve as an example of the economic damage caused by this catfish (Mendoza et al. 2007).
In the Alvarado Lagoon system, populations of exotic species were intentionally introduced for fishery development purposes. This is the case of Oreochromis aureus, O. niloticus and Coptodon zillii, whose populations in the Papaloapan basin were a consequence of the massive importation from Alabama, United States, carried out in 1964 by the National Institute of Biological-Fisheries Research at the Tropical Aquaculture Station in Temascal. On this institute, experimental farming of several native species (Ictalurus sp.) and translocated species, such as the cichlids Bay snook Petenia splendida and the Mexican mojarra Mayaheros urophthalmus was carried out (Delgadillo-Tiburcio 1976). There species likely have escaped to the Papaloapan River basin and dispersed to the Alvarado Lagoon (Chávez-López et al. 2009).
Imbalances in ecosystems and severe socio-economic impacts are commonly reported for many exotic species worldwide (Gozlan et al. 2010), with introduction and establishment prevention being considered as the most efficient measures to avoid the impacts. While actions to control the introduction of non-native species exist in the Mexico, these are, unfortunately, insufficient. A way to improve them is coordination and implementation of the national strategy on invasive species in Mexico (Comité Asesor Nacional sobre Especies Invasoras 2010), with the guidance of local authorities SEMARNAT and CONABIO (institutions whose primary purpose is acknowledging biodiversity and ensuring the preservation of natural resources in Mexico). As a measure to prevent further non-native species introductions in Mexico, we suggest permanent inspection by the environmental authorities to the aquaculture production sectors, prompt notification of recent introductions, application of the Polluter Pay Principle to producers or officials responsible for introductions of species and elimination or control of propagation of non-native species.