Exotic and invasive fishes in Mexico

This paper presents a list of the exotic fish species introduced in Mexican aquatic systems. This list is the result of the systematized information contained in several databases of ichthyological collections around the world and different publications. A total of 104 species were found, distributed in 19 families and 51 genera. The most species-rich were Cyprinidae with 22 species, Poeciliidae (19 species), Cichlidae (15 species) and Centrarchidae (13 species). A map and an electronic database were created based on the knowledge of the species, showing the known introductions of exotic fishes in the country. The information was obtained from a database stored in the Colección Nacional de Peces IBUNAM, which can be accessed online. This study has a high importance for the knowledge of the exotic fish fauna of Mexico and its current status.


INTRODUCTION
Fish are the most diverse group of vertebrates, and freshwater fish are especially considered as one of the most seriously threatened animal groups, because of the introduction of exotic species (non-native), it means, species that do not belong naturally to an aquatic system (CONABIO 2008).These species cause damage to ecosystems by the deterioration of the water body, and strong effects on native communities in which they are inserted (Contreras-Balderas 1999).The introduction pathways of fish and other organisms may be deliberately, for purposes of aquaculture, sport fishing, biological control or protection of species and forage, or accidentally including leakage of individuals from farms, discharge ballast water, hydrological systems channeling and the release of species used as bait in a different system from where they were collected (Gozlan et al. 2010).
Frequently, introduced or exotic species are mistaken as invasive species, the latter considered as those whose abundance and distribution are significantly greater than when the species was first introduced.Although the term is widely used, there is no clear definition to designate a species as invasive, as there is some subjectivity in its use (Wittenberg et al. 2001).For practical purposes, this paper defines invasive fish as non-native species that, once introduced to a water system, its reproductive success allows it to establish and significantly increase its distribution.This contribution aims to update the list of invasive species of Contreras-Balderas (2008), and includes a list of invasive species and their effects on introduction environments.An interactive database, stored electronically in the Colección Nacional de Peces of Instituto de Biología UNAM, which can be consulted online.
Espinosa-Pérez and Ramírez | Exotic and invasive fishes in Mexico show the records of introduced fish species reported by Contreras-B and Escalante-C (1984) and Contreras-Balderas (1999).The localities in which the introduced species were observed or collected, as well as the number of records by locality of the selected species are also shown.
Lepisosteidae: Although four species of this family are native to Mexico and North America, from Canada to Nicaragua, at least Lepisosteus osseus (Linnaeus, 1758) is known to be imported from the United States, where it is stocked for conservation purposes.In Mexico, stocking of this specie is done for sport-fishing and riverine fishing in Tamaulipas dams (García de León et al. 2005).
Clupeidae: Data of introduction or translocation of Dorosoma cepedianum (Lesueur, 1818) and D. petenense (Günter, 1867) in rivers, lakes and reservoirs in the north of Mexico are available according to Contreras-B and Escalante-C (1984).These species are native to the Atlantic coast, northeast and southeast of Mexico, but have been introduced as forage species for food to other species such as Largemouth Bass (Micropterus salmoides (Lacepède, 1802)).Currently there are more records of these two species in the northern and southern regions of the country, but the effects in native populations are not known.
Chanidae: The species Chanos chanos (Forsskål, 1775) was introduced in America by the end of the last century in the San Francisco estuary, United States of America, where according to Castro-Aguirre et al. (1999) it does not occur.Its current distribution extends from the southwestern coast of Baja California Sur and the Gulf of California to Panama and Galapagos Islands, and in lagoons of Sinaloa, Nayarit, Jalisco, Guerrero and Chiapas, in Mexico.This species is native to the Red Sea and the Indian Ocean.
Cyprinidae: Twenty-two species of this family have been recorded as non-native, introduced on Mexican water bodies, many of them are translocations or unverified records of Mexican species in other systems.Among them are: Algansea lacustris Steindachner, 1895, introduced in many aquatic systems in central Mexico.It is unknown whether the species is established or not, but there is suspicion that it has hybridized with other species of the genus (Escalante and Contreras 1985).Cyprinella lutrensis (Baird & Girard, 1853) was documented by Contreras-Balderas et al. (2008) as introduced, and mentioned it in multiple localities in the north.Ruiz-Campos et al. (2012) suggested the species to be probably responsible of the decline of the Desert Pupfish Cyprinodon macularius Baird & Girard, 1853.Other species such as Gila bicolor (Girard, 1856), G. modesta (Garman, 1881) and G. orcutti (Eigenmann & Eigenmann, 1890) natives from the United States were documented by Contreras-B and Escalante-C and Smithsonian Institution, Washington, DC (USNM).A great number of the records (3478) were taken from the database CONABIO recorded by Contreras-Balderas (2008) and from the records obtained online from public and international databases such as Global Biodiversity Information Facility (GBIF) and the FishNet data portal (FishNet2.net),which gather numerous references of various species throughout the world.Literature and faunal lists were also reviewed, such as Ruiz-Campos et al. (2012), which include records of exotic species in the peninsula of Baja California, the faunal list Contreras-B and Escalante-C (1984), Contreras-Balderas (1999) or Mendoza and Koleff (2014).
A map and an interactive database were done with all data obtained from the databases.Entries were standardized, overlapping records were eliminated and spelling errors were corrected.Records with accurate geographical coordinates were used; coordinate acquisition of each locality was achieved a posteriori by mapping and matching (less than 10 m in diameter) the collection site to a water system.For this purpose the online service GEOLocate and Fishnet2 were used, as well as GIS Google Earth 6.0.Fish nomenclatures were verified according to recent taxonomic revisions, following the arrangement of Page et al. (2013) and the Catalog of Fishes (Eschmeyer and Fong 2014).The list of introduced and exotic species in Mexico is shown in Table 1, with their native distribution the area of occurrence in Mexico including known distributions and samples of collection, the causes of the introduction, the current status of invasion and the catalog number of the specimens deposited in fish collections.The species are listed in four categories: exotic, introduced, invasive and required to verify."Exotic" includes foreign species sensu stricto, those that comes from other countries."Introduced" refers to species that have been introduced in a water system by anthropogenic purposes, such as aquaculture, and those species that were translocated due to sport fishing, bait, or reintroduced for conservation purposes."Invasive" refers, as in the introduction, to those species that have established and are widely distributed in different water bodies of Mexico."Requires verification" concerns to those species not deposited in a scientific collection, as M. anguillicaudatus (Cantor, 1842).This category also includes those species whose distribution overlaps their native distribution.

RESULTS
Nineteen families, 59 genera and 104 species of exotic fish have been introduced in the Mexican water systems.An analysis of the families of all species reported is presented below.The database and electronic map presented in this work can be consulted online using the link http://unibio.unam.mx/peces_exoticos-war/,and Espinosa-Pérez and Ramírez | Exotic and invasive fishes in Mexico (1984) in Baja California, but these species were not found by Ruiz-Campos et al. (2012).Campostoma anomalum (Rafinesque, 1820), Macrhybopsis aestivalis (Girard, 1856), Notropis chihuahua Woolman, 1892, N. amabilis (Girard, 1856), Pimephales promelas Rafinesque, 1820 andP. vigilax (Baird &Girard, 1853) were also documented as introduced species, possibly used as bait by fishermen, but no recent records was found (Contreras-Balderas, 1999).Notemigonus crysoleucas (Mitchill, 1814) inhabits waters in the Rio Grande basin, mainly in Tamaulipas.The only two records from Lee et al. (1980) on the coast between California and Arizona are not enough to conclude that the species is established.The remaining 11 species of Cyprinidae are exotic to the country, naturally from India, Sri Lanka and China.Two of these species: Pethia conchonius (Hamilton, 1822) and Puntius titteya (Deraniyagala, 1929) were introduced for ornamental purposes and their status is unknown, although Contreras-B and Escalante-C (1984) mentioned them as probably established in Nuevo Leon (northern Mexico), but no recent record has confirmed this information.However, a new record of P. conchonius was recently found in a dam in Guerrero (southern Mexico) and the specimen was deposited with the catalog number in CNPE-IBUNAM 20010.The other exotic cyprinids were introduced mainly by accidental releases of aquaculture (Ibáñez et al. 2011)  Catostomidae: Carpiodes carpio (Rafinesque, 1820) was reported by Hendrickson et al. (1980) in Presa Novillo where it was extremely common in shallow areas in the early seventies.Its distribution is from Mississippi basin from Pennsylvania to Montana, south to the Gulf of Mexico drainages from the Mississippi River to Mexico (Contreras-B and Escalante-C 1984), therefore could be considered as translocated species, nevertheless its status is currently unknown.
Cobitidae: Misgurnus anguillicaudatus (Cantor, 1842) from Asia is considered of high risk to the native Mexico species, for its easy adaptation to almost any aquatic environment and its high rate of depredation.In Mexico it was introduced in the sixties into the channels of Chapingo, State of Mexico, due to its potential for aquaculture.It is apparently not established due to water pollution and loss of habitat in the region (Contreras-B and Escalante-C 1984).
Loricariidae: Pterygoplichthys disjunctivus (Weber, 1991), P. multiradiatus (Hancock, 1828) and P. pardalis (Castelnau, 1855) have been recorded in Mexican freshwater environments and were apparently introduced due to releases from farms or aquariums (Gozlan et al. 2010).These fishes were reported in Mexico since 1995 in Presa Adolfo Lopez Mateos, Michoacán and recently Wakida-Kusunoki et al. (2007) mentioned that they are distributed in Campeche, Chiapas and other localities of central and western Mexico.Although according to Mendoza et al. (2008) the Pterygoplichthys specimens found in Mexico may represent a complex of six species that have not been adequately addressed.Espinosa et al. (2011) show how to diagnose two of these species from Chiapas.From 1995 to date, this group has been fully established and expanded their distribution in Mexican rivers and reservoirs.
Ictaluridae: Five species of this family have been introduced in Mexican water systems for aquaculture.Ictalurus furcatus (Valenciennes, 1840) is distributed in the Atlantic coastal drainages from the Mississippi River to Guatemala, and also documented in the Pacific, in the Yaqui River and in the peninsula of Baja California, according to Contreras-B and Escalante-C (1984).I. punctatus (Rafinesque, 1818) is distributed in northern Mexico in the Atlantic slope, and has been introduced due to its intensive farming in many parts of the world.In Mexico it is known to occur in dams, lakes and rivers of central and northern Mexico, where it is fully established.Ameiurus melas (Rafinesque, 1820) and A. natalis (Lesueur, 1819) do not occur naturally in Mexico, but they have been introduced in many rivers for aquaculture, where they have established according to Contreras-B and Escalante-C (1984) who reported them in different localities of the Rio Pánuco, Lerma-Santiago and Balsas.Pylodictis olivaris (Rafinesque, 1818) is now established in the lower Rio Colorado basin, including parts of Baja California and Sonora (Miller et al. 2009).The only voucher specimen is from northwestern Mexico was captured in the junction of the Rio Colorado and Rio Hardy (Ruiz-Campos et al. 2012).
Salmonidae: There is no consensus about the number of undescribed native species of this family in Mexico (Hendrickson et al. 2002).The introduction of Salvelinus fontinalis (Mitchill, 1814) in the sixties in the State of Mexico was unsuccessful, and there are no recent records of its establishment.Oncorhynchus mykiss (Walbaum, 1792) was introduced in several parts of the country, although part of its native distribution is in the northwest of Mexico (Miller et al. 2009).This species is Espinosa-Pérez and Ramírez | Exotic and invasive fishes in Mexico fully established in many mountain areas of the country.Currently, the presence of the Brown Trout, Salmo trutta Linnaeus, 1758 is known only from several farms in states of Mexico and Puebla.
Atherinopsidae: Nine species of this family were translocated and introduced in different water environments in the country, mainly to serve as fodder for other introduced species such as bass, catfish and trout.Only in some cases, Chirostoma sphyraena Boulenger, 1900 and C. estor Jordan, 1880 are used as food.These introductions caused great inconvenience to taxonomists, who nowadays face several problems to determine species such as hybridizations.Other species, such as C. aculeatum Barbour, 1973, C. consocium, C. grandocule (Steindachner, 1894), C. jordani Woolman, 1894, C. labarcae Meek, 1902, Membras martinica (Valenciennes, 1835) and Menidia beryllina (Cope, 1867) were introduced into water bodies in northern Mexico with unknown results of such introductions (Miller et al. 2009).
Fundulidae: Two species of this family, Fundulus zebrinus Jordan & Gilbert, 1883 and F. grandis Baird & Girard, 1853 have been recorded as introduced.Fundulus zebrinus was reported by Contreras-B and Escalante-C (1984) in three localities in the middle Rio Grande whereas Fundulus grandis is distributed in Veracruz and Tamaulipas, although in Nuevo Leon and Chihuahua could be present according Contreras-Balderas (2008).
Poeciliidae: Nineteen species are considered introduced or translocated.Gambusia affinis (Baird & Girard, 1853) is native from Mississippi River basin from central Indiana and Illinois, south through the Golfo de México drainages and northern Veracruz (Page and Burr 1991).It was introduced in different system waters since 1931 as part of a mosquito control program.The first place where it was reported is in Arroyo San José, Baja California by Miller and Hubbs (1954), later Ruiz-Campos et al. ( 2012) report it again in many localities of Baja California, also it has been found mostly in some northern states of the country (Figure 1).
There are other five species of this genus (G. hurtadoi Hubbs & Springer, 1957;G. panuco Hubbs, 1926;G. regani Hubbs, 1926;G. senilis Girard, 1859 andG. speciosa Girard, 1859) which have been translocated due to aquaculture or accidental release; in most cases the current status of invasion is unknown.Also it was found six species of the genus Poecilia (P.butleri Jordan, 1889; P. latipinna (Lesueur, 1821); P. latipunctata Meek, 1904;P. mexicana Steindachner, 1863 andP. reticulata Peters, 1860) five of this species are native, and have been translocated from one system to another, mainly by aquarists and by government nutrition programs.Whereas the guppy (P.reticulata Peters, 1859), is a native species from Guyana and Venezuela used as aquarium fish, is the most invasive exotic fish in the freshwater bodies of the central and southern Baja California Peninsula (Ruiz-Campos et al. 2012).Heterandria bimaculata (Heckel, 1848) is originally restricted to the Atlantic slope, but currently it can be found in several localities in the Pacific slope, mainly in the Balsas River basin the cause of its introduction is unknown although some authors mention aquaculture or accidental releases as probable causes (Contreras-Balderas 1999, Miller et al. 2009).The same was observed for Poeciliopsis gracilis (Heckel, 1848), but the limits of its dispersion are known, although it is thought to have hybridized with other species of the genus (Courtenay and Maffe, 1989).Seven species of the genus Xiphophorus (X.couchianus (Girard, 1859); X. gordoni Miller & Minckley, 1963;X. hellerii Heckel, 1848;X. maculatus (Günther, 1866); X. meyeri Schartl &Schröder, 1988 andX. variatus (Meek, 1904)) are spread in the water systems of the country due to aquarists, or have been transported with cichlids at different sites of the country, as well as with Astyanax and Poecilia species (Espinosa et al. 2011).
Cyprinodontidae: Cyprinodon variegatus Lacepède, 1803 was reported by Contreras-Balderas (2008) as an introduced fish.However its natural distribution is between the towns showed in Table 1.Hence, more surveys are necessary to assess this information.
Scorpaenidae: Only one species of this family, Pterois volitans (Linnaeus, 1758), native to the Indo-Pacific region, has been introduced into Mexican marine waters and are known to have invaded the Caribbean in Florida, where it was originally introduced.This species is a several threat to Caribbean reefs, where it has no natural competitors or predators (Betancur et al. 2011).
Moronidae: The two species of this family recorded in Mexican water bodies are Morone chrysops (Rafinesque, 1820) and M. saxatilis (Walbaum, 1792), both native to the Atlantic coast of the United States belonging to the wildlife of the template American Atlantic.M. chrysops is native from Mississippi River and Ohio valleys.Contreras-B and Escalante-C (1984) reported it in lower and middle Rio Grande also in Rio San Juan to Dr. Coss, Nuevo Leon, with aquaculture purpose and sport fishing, whereas M. saxatilis is natural from the coastal drainages and littoral marine waters of the Atlantic, from St. Lawrence River in Canada to the south of St. Johns River in Florida (Ross 2002).Contreras-Balderas (1999) reported it in Rio Bravo and mentioned as causes of its introduction the aquaculture and sport fishing, and Mendoza et al. (2011) mentioned that this species are causing a several decrease in the native fishes of Laguna Madre because it is a voracious depredator.
Centrarchidae: Even though there are four native species in this family particularly from the Rio Grande basin (Lepomis cyanellus Rafinesque, 1819; L. macrochirus Rafinesque, 1819; L. megalotis Rafinesque, 1819 and Micropterus salmoides (Lacepède, 1802)), Sunfishes have been introduced in the north of the country for different reasons, but mainly as part of aquaculture projects.All introduced Centrarchidae species are known to be established, but the range of their distribution is unknown.This is the case of the two species of Pomoxis (P.annularis Rafinesque, 1818 and P. nigromaculatus (Lesueur, 1829), it is known that in Durango both species are completely dominant in rivers and dams causing several damages on the native fishes (Garcia de León et al. 2005).
Sparidae: In 2004, the transnational company Biotecmar S.A. received permission from the Mexican environmental authorities to establish a commercial culture of seabass in Bahía de La Paz, on the southwestern side of the Gulf of California.In September 2005, instead of introducing seabass, the company introduced at least 300,000 individuals of the gilt-head seabream Sparus aurata Linnaeus, 1758.On 3 October 2007 an individual of S. aurata was captured in the wild during experimental fishing work in the Bahía de La Paz in the Golfo de California.This fish has invaded large areas of the Mar de Cortes due to its escape (Balart et al. 2008).
Sciaenidae: Aplodinotus grunniens Rafinesque, 1819 was reported as introduced by Contreras-Balderas (2008).Its native distribution is along the Atlantic slope drainages in Mexico, for this reason the records in Coahuila and Nuevo Leon are considered to represent traslocation.Sciaenops ocellatus (Linnaeus, 1766) is a marine-estuarine species, distributed in the coastal area from Massachusetts to Veracruz, introduced in the Laguna of Términos in Campeche for fishing purposes.The establishment of the species in Laguna of Términos is unknown (Wakida-Kusunoki and Santos-Valencia 2008).
Cichlidae: Within this family there are more than 40 native species in Mexico, of which Cichlasoma urophthalmus (Günther, 1862), Herichthys cyanoguttatus Baird & Girard, 1854, Petenia splendida Günther, 1862, Rocio octofasciata (Regan, 1903), Thorichthys ellioti Meek, 1904 andTheraps pearsei (Hubbs, 1936) have been mentioned as introduced or translocated to several localities of the country.These are the cases of Cichlasoma urophthalmus and Petenia splendida, spread further their natural range of distribution in Chiapas and Oaxaca.Herichthys cyanoguttatus was registered as traslocated by Contreras-Balderas ( 2008), in different waters bodies.Some authors mentioned that this species has already hybridized with a native closely related species in Cuatro Cienegas, Coahuila, however this has not been well documented (Husley et al. 2003).Parachromis managuensis (Günther, 1867) and Parachromis motaguensis (Günther, 1867) are native species from Central America and were probably introduced to water bodies in the southeastern Mexico, and are now fully established in the Grijalva-Usumacinta basin (Miller et al. 2009).Amatitlania nigrofasciata (Günther, 1867) is a native species from Central America including the Pacific slope from Rio Sucio and it is considered ornamental.Figure 2

DISCUSSION
In this work we reported 104 introduced fish species in Mexico, grouped into 19 families and 59 genera, representing 3.76% of the fish diversity of the country according to Espinosa-Perez (2014).Of 104 introduced Espinosa-Pérez and Ramírez | Exotic and invasive fishes in Mexico species, 62% are established with a wide distribution in the country, such as the Common Carp (Cyprinus carpio) and the Bream (Oreochromis and Tilapia), herein considered invasive.Forty two species are foreign, mainly natural from Asian, European and North American, and the remaining is considered translocated species.Translocation is defined here as a native species from a determined aquatic system in Mexico that has been introduced in other localities, such as some cichlids and poecilids (Theraps pearsei, Rocio octofasciata, Amatitlania nigrofasciata, and some species of the genera Poecilia and Gambusia).
Furthermore 20% of the species reported in this work are species of freshwater environments; this means that in the case of marine species, there is not enough information about the introduced species.Only the Lionfish (Pterois volitans Linnaeus, 1758) is mentioned to be widely spread in the coasts of the Golfo de Mexico and the Caribbean.There are many studies about the behavior, development, habits, genetic, effects on the environment in which it is introduced or impact on native species about this fish.Currently its eradication is considered impossible or nearly impossible due to the absence of natural depredators to control the population of this species.One alternative is the implementation in the Mexican food of this fish, some institutions like Comision Nacional de Areas Protegidas (CONANP), Secretaría del Medio Ambiente y Recursos Naturales (SEMARNAT) and the Veracruz government compiled a recipe book with the purpose of promoting the consumption of this fish in the local people and tourists.
Of the total species reported in this work, 31.4% is represented mainly by four freshwater fishes, two of them Asian natives (Cyprinus carpio and Oreochromis niloticus).The Common carp (C.carpio) represent 10.68%, while Largemouth Bass (Micropterus salmoides) 7.71%, and Nile Tilapia (O.niloticus) 7.61% and the Shortfin Molly (Poecilia mexicana) 5.4%.The first one is species used within aquaculture purpose, it was found that this is the main cause of introduction (29%), moreover there are species as the two others (M.salmoides and P. mexicana) that are used as ornamental fish or sport fishing purpose, these causes represent 15% and 12% respectively.These are not the only introduction causes, it was found that the introduction of foraging species and accidental release also represents the 12%.Only four causes represent less than 10% among them are reintroduction, it was the case of Gila modesta (Garman,1881); with protection purpose like the case of G. orcuttii (Eigenmann & Eigenmann, 1890) and Siphateles bicolor (Girard, 1856) while Ctenopharyngodon idella and Gambusia affinis as mentioned were introduced with bait purpose (Contreras-Balderas 1999).There is no information about the introduction of the remaining species.Therefore, they were grouped in the category "require to verify" on Table 1.
A contribution of this work is the inclusion of the Milkfish (Chanos chanos (Forsskål, 1775)) to the list of introduced species of Mexico.This fish is a native species from the Indo-Pacific of the family Chanidae and even though it was previously reported by Castro-Aguirre et al. (1999), it has not been considered officially as an introduced species in Mexico.According to this author, this fish was introduced to North America by the end of the last century in the San Francisco estuary for aquaculture purposes or accidental releases from the farms in the United States.The current inclusion of this species on the list is supported by specimens collected in coasts of Nayarit and deposited in the CNPE-IBUNAM (Table 1).
Another contribution is that we report the presence of the brown trout (Salmo trutta) in hatcheries of the state of Mexico and Puebla.This species had only been reported by Hendrickson in the early 1980s near Yaqui River in the north of Mexico, and was not mentioned in any other publication.The specimens in which we base our report were deposited in the Colección Nacional de Peces of the Instituto de Biología of UNAM with catalog number 18454 CNPE-IBUNAM.
The purpose of the electronic resources is to be able to follow up on the current situation of these species through constant update of the data.The update is possible with the help of researchers and people interested in fish introductions, and the contact with the Colección Nacional de Peces of the Instituto de Biología UNAM in Mexico through the e-mail cnpe@ib.unam.mx.Data sent in for inclusion in the database must include the locality or the place where the fish was seen or collected, the exact geographic coordinates, and a clear photograph showing the morphological characteristic of the fish.With this information we will be able to determine if it is a new record or not.

Figure 1 .
Figure 1.Traslocated distribution of Western Mosquitofish (Gambusia affinis) in northern country due to mosquito control programs.
shows some records of this fish in Mexico.It is established and widely disseminated throughout the country mainly in the center and southeast of Mexico(Mendoza and Koleff 2014).Oreochromis aureus (Steindachner, 1864), O. mossambicus (Peters, 1852), O. niloticus (Linnaeus, 1758), Tilapia rendalli (Boulenger, 1897), T. zillii (Gervais, 1848) and Hemichromis guttatus Günther, 1862 are African species introduced for aquaculture in Mexico.These species have been progressively introduced in many freshwater bodies of the country, both natural and artificial for aquaculture and commercial catch.Its high capacity of competition for resources like space and food has caused the displacement of native fishes as the case of Cyprinodon macularius Baird & Girard, 1853, in the lower Rio Colorado basin of Baja California and Sonora(Varela- Romero et al. 2003).

Figure 2 .
Figure 2. Map of different records of Amatitlania nigrofasciata observed or captured in Mexico.
* suggest exotic species from other countries.