Fishes of the Grijalva River basin of Mexico and Guatemala

The Grijalva River basin is one of the largest hydrological systems in Central America. Despite its importance, an inventory of its ichthyofauna remains incomplete. We provide a systematic checklist of fishes recorded in the Grijalva River basin based on surveys performed from 2002 to 2015. The systematic list includes 92 species, belonging to 13 orders, 25 families and 50 genera, of which 83 species are native and nine are exotics. This checklist includes three range expansions (Profundulus hildebrandi, Poecilia sphenops and Paraneetroplus hartwegi). Fifteen species are endemic to the basin. The most diverse families are Cichlidae and Poeciliidae with 25 and 23 species, respectively. Secondary freshwater fish diversity is high with 65.1%, the remaining species are primary freshwater (13.3%) and peripheral (21.7%) fishes.


INTRODUCTION
The Grijalva-Usumacinta basin is the largest river system in Central America and it is considered a hotspot of biodiversity (Hudson et al. 2005).In Mexico, although the drainage represents only 4.7% of the total surface area, its ecosystems contain 64% of all biodiversity (Toledo 2003).The Grijalva River basin has been severely modified due to damming, and this is one of the major threats to the fish fauna.In addition, water pollution, siltation, overfishing, and introduction of exotic fishes continues to threaten fishes of this region.
Although the Grijalva River has high species richness and high levels of endemism (Rodiles-Hernández 2005;Velázquez-Velázquez et al. 2013), species composition lists remain incomplete and are restricted to smaller geographic areas, mostly near dams and protected areas (e.g., Bueno-Soria and Santiago-Fragoso 2002;Olmos-Tomasini 2002;Pérez et al. 2002;Rodiles-Hernández 2005;González-Díaz et al. 2008).The aim of this study was to describe the composition and distribution of the ichthyofauna throughout the entire Grijalva River basin.

Study area
The Grijalva River is located in southern Mexico and northwestern Guatemala.Together with the Usumacinta River, it is the most voluminous river system in Mesoamerica (Tamayo and West 1964).The Grijalva River basin covers an area of 58,000 km 2 , of which 9% are in the upper reaches of the Sierra de los Cuchumatanes, Guatemala and the remaining portion in Mexico, throughout the states of Chiapas, Tabasco, and small portions of Oaxaca and Veracruz, until it joins with the Usumacinta River and drains into the Gulf of Mexico (Hudson et al. 2005; García-García 2011; Figure 1).
The Grijalva River basin is divided in three hydrological regions: Upper Grijalva or Grijalva-La Concordia, Middle Grijalva or Grijalva-Tuxtla Gutiérrez and Lower Grijalva or Grijalva-Villahermosa (SEMARNAT 2010a; Figure 1).In the state of Chiapas, the main channel of the river has been highly modified due to the construction of four large hydroelectric dams: Belisario Domínguez or La Angostura, Manuel Moreno Torres or Chicoasén, Nezahualcóyotl or Malpaso, and Ángel Albino Corzo or Peñitas (Figure 1).

Fish sampling
More than 200 sampling stations were surveyed throughout the Grijalva River basin since 2002 (Figure 1).The bodies of water sampled included streams, lagoons, points along the main river channel, near dams, as well as underground waters, that were selected to maximize the diversity of the sampled environments in order to represent the complete composition of the

RESULTS
The fish fauna of the Grijalva River basin is composed by 92 species, belonging to 13 orders, 25 families and 50 genera, of which 83 species are native and nine are exotics.From the total, 77 species are deposited in our vouchers and 15 are literature records.The orders Perciformes and Cyprinodontiformes are the most diverse groups, with 36 and 28 species, respectively (Table 1), both representing 69.6% of the total richness.Cichlidae is the most diverse family, with 25 species (30.1% of total richness, not including exotics), followed by Poeciliidae with 23 (27.7% of total richness;  2).

DISCUSSION
The Grijalva River basin together with the Usumacinta are included within the Usumacinta ichthyological province (sensu Miller 1966, but see Matamoros et al. 2015), which shows the highest levels of freshwater fish diversity and endemism in Central America (Miller 1966;Myers 1966;Bussing 1998;Matamoros et al. 2015).Miller et al. (2005) recognized nearly 200 species in this province, and 115 species throughout the complete Grijalva-Usumacinta basin.This highlights the great diversity in the Grijalva basin, which comprises almost half of the total richness of this province.The high diversity found in this region is due to a complex geological history and the recent connections between the Grijalva River and adjacent basins (González-Díaz et al. 2008).As a result, some species are restricted to particular habitats; Rhamdia laluchensis and R. macuspanensis that are stygobitic, and several species of poeciliids inhabit in sulphidic ambients, as Poecilia sulphuraria, P. thermalis and Gambusia eurystoma.Despite its importance, the Grijalva River basin has not received substantial study.As a result, several new species have been discovered in the basin in the last 35 years, such as Paraneetroplus hartwegi (Taylor & Miller, 1980), Cichlasoma grammodes Taylor & Miller, 1980, Poeciliopsis hnilickai Meyer & Vogel, 1981, Thorichthys socolofi Miller & Taylor, 1984, Heterophallus milleri (Radda, 1987), Paraneetroplus breidohri (Werner & Stawikowski, 1987), Rhamdia macuspanensis Weber & Wilkens, 1998, Rhamdia laluchensis Weber, Allegrucci & Sbordoni, 2003, and Priapella chamulae Schartl, Meyer & Wilde, 2006; also recently, some species previously considered endemics to the Coatzacoalcos river basin have been recorded in the middle section of the Grijalva basin, including Paraneetroplus regani, Priapella intermedia, and Xiphophorus clemenciae (González-Díaz et al. 2008;Gómez-González et al. 2014).Also, some cichlids, such as Amphilophus macracanthus and Cichlasoma trimaculatum, formerly only known in the Pacific drainage, have shown up in the Grijalva, although apparently the latter for both may be a recent translocation (Miller et al. 2005).
Recently, we discovered another population of the San Cristóbal Pupfish (Profundulus hildebrandi) in the upper reaches of the Teapa-Tacotalpa system, in the municipalities of San Juan Chamula and Chenalhó, Chiapas.This species is considered microendemic; its habitat is being encroached upon by urban growth in the Valley of San Cristóbal de Las Casas, Chiapas, so it is considered endangered by Mexican law (Contreras-Balderas et al. 2003;Velázquez-Velázquez and Schmitter-Soto 2004;Velázquez-Velázquez et al. 2008).The new record of this population expands its geographic range.
We expanded the known distributional range of Paraneetroplus hartwegi that has long been considered endemic to the upper Grijalva (Miller et al. 2005).González-Díaz et al. (2008) found that this species is common and abundant in the middle Grijalva in La Venta River basin and Malpaso Reservoir.Recently we found it in rivers and streams of the lower basin.Because of its abundance and distribution it may be necessary to reassess its conservation status, presently considered as threatened by Mexican law.Poecilia sphenops has disjunct populations; it is distributed in rivers, streams and brackish lagoons of the Pacific coastal plain, but also in the Middle and Upper Grijalva and in the Coatzacoalcos River basin (Schultz and Miller 1971;Miller et al. 2005;González-Díaz et al. 2008); this species was collected in the upper parts of the Teapa-Tacotalpa and Tulijá-Macuspana systems, it occurs in sympatry with Poecilia mexicana but not in syntopy: whereas P. mexicana inhabits rivers and streams with fast flow, clear water and high concentration of dissolved oxygen, P. sphenops is found in ponds and lagoons without flow, high turbidity and low oxygen levels.
The species richness in the Grijalva River basin is lower in the upper parts and increases in the lower portions.The lower Grijalva is the most diverse region, due to the presence of peripheral species and components shared with the Usumacinta River.The upper basin has been severely affected by hydroelectrical power development; as a result, the distribution of some species has been altered, reduced, or eliminated.The isolation and the change of hydrological conditions caused the disappearance of migratory species such as Agonostomus monticola¸ mentioned by Taylor and Miller (1980), although actually there are no vouchered records.Centropomus undecimalis also penetrates to the middle section of the river, according to local fishermen.Presently, other species are very rare in the basin upper reaches, as is the case of Ictiobus meridionalis, Eugerres mexicanus, and Aplodinotus grunniens, but they are very common and abundant in the basin lower reaches, especially in the Tulijá-Macuspana system.
The secondary component is represented, with 54 species (65.1% of native species), mainly cichlids and poeciliids, the dominant families in most Central America river systems (Miller 1966(Miller , 1982;;Myers 1966;Bussing 1998;Matamoros et al. 2015).Primary fishes are poorly represented, with only 11 species (13.3%), and marine derivatives with 18 species (21.7%), especially vicarious forms (species derived from marine ancestors, actually restricted to freshwater habitats).This paucity of primary freshwater fishes is also present in most basins of Central America, whereas in North and South America the fish fauna is dominated by ostariophysans, such as carps and minnows to the north and catfishes, characins, and knifefishes to the south (Miller 1966;Myers 1966;Bussing 1985;Smith and Bermingham 2005;Chakrabarty and Albert 2011;Matamoros et al. 2015).
Exotic species comprise an important source of food and are economically valuable in the upper basin, especially Nile Tilapia, Oreochromis niloticus, a fish widely distributed and found in almost all areas throughout the Grijalva basin.Tilapia zillii, another exotic cichlid, and O. niloticus are very common and abundant in the Upper Grijalva, mainly in La Angostura reservoir, in Gómez-González et al. | Fishes of Grijalva River which both sustain local fisheries and represent more than 50% of capture efforts.The abundance of exotic species seems to gradually decrease in the lower reaches of the basin, in which native species as Petenia splendida, Ictalurus meridionalis, Atractosteus tropicus and many native cichlids comprise the catch of local fisheries.Another problem related to exotic fishes in the upper section, especially with the Common Carp (Cyprinus carpio), is the presence of non-native parasites such as the Asian Tapeworm (Bothriocephalus acheilognathi), recently recorded in the endemic pupfishes Profundulus candalarius (pers.obs.) and P. hildebrandi (Velázquez-Velázquez et al. 2011).The Asian Parasitic Copepod (Neoergasilus japonicus) has been reported in the endemic cichlids Cichlasoma grammodes, Paraneetroplus breidohri, and P. hartwegi (Suárez-Morales et al. 2010); most of the parasitized species are included in a risk category according to Mexican law (NOM-059-SEMARNAT-2010), but it will be necessary to assess the presence of these exotic parasites in other native species.In the Lower Grijalva, the Armored Catfish (Pterygoplichthys spp.) represents a serious risk for the native fish fauna and the whole ecosystem, due to its high abundance and widespread distribution (Wakida-Kusunoki et al. 2007;Liénart et al. 2013).Additional effort is needed to attempt to control or eradicate the spread of this invasive species.
In conclusion, the present survey provides information for the monitoring of fish fauna and management of fishing resources in the Grijalva River basin, a highly diverse and economically important region in Middle America.

Table 1 .
Taxonomic composition of the ichthyofauna of the Grijalva River basin.Names in bold indicate the most diverse taxa.