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Identification of three Ictalurus species in Mexico using Cytochrome Oxidase I gene sequencing.

Mexico contributes with nearly 10% of the world fish diversity (CONABIO, 2014). 543 out of 3000 species are subject to commercial exploitation in the country (SAGARPA, 2013). However, it has been proposed that 86% of the species on Earth and 91% in the ocean still need to be described (Mora et al., 2011). Channel catfish Ictalurus punctatus is one of the Mexican freshwater fishes with the highest presence in American aquaculture. For its exploitation on aquaculture and fisheries, channel catfish have been introduced in 20 states of the Mexican territory (Lara-Rivera et al., 2015). Reservoirs are common receptacles for fry and adult releases in order to promote local subsistence fishing. Since there are no reports of neither prior nor subsequent studies of these releases, it is uncertain if wild and domestic populations have mixed at some point. On the other hand, fishermen are not familiar with the taxonomical distinctive characteristics of the different species of the genus Ictalurus, which leads to misidentification of fish from the net and all the way to the market. In order to identify a specimen, there is need of two things: first, a specialized taxonomist, and second, specimens in an ideal state of preservation. DNA barcoding has proven to be a powerful tool for rapid, non-morphological and accurate species identification and discovery (Ward et al., 2005). Sequencing of a 648 bp region from the Cytochrome Oxidase 1 (COI) region allows comparison and identification of species based on similarities among related groups (Clare et al., 2007). Among the most useful applications of DNA barcoding are identification of fish products and sub-products (such as fillets, nuggets and conserves), mislabeled products (Jacquet & Pauly, 2008; Wong & Hanner, 2008; Galal-Khallaf et al., 2014) and recognition of endangered or potentially risky species (Galimberti et al., 2013; Quinto et al., 2016). There is very few information regarding channel catfish distribution on Mexican continental waters and nowadays, I. punctatus is considered to be an invasive species in Mexico (Gonzalez et al., 2014), since the production began from fish imported from the USA instead of Mexican native populations. Therefore, the aim of the present work was the molecular identification of Mexican catfish using a DNA barcoding approach.

A total of 93 samples were used for the analysis (Table 1); 17 samples representing the most important aquaculture farms in Mexico, 70 samples were obtained from free-living catfish from 5 reservoirs, 5 rivers, and 1 lake. Additionally, 5 commercial samples, labeled as "catfish" were used for a comparative analysis. Samples consisted of anal and adipose fins. DNA was extracted using the commercial kit GenElute Mammalian Genomic DNA Miniprep (SIGMA Aldrich[R]) following the directions provided by the manufacturer. DNA integrity was verified on 1.5% agarose gels. DNA concentration was calculated using a Nano Drop 2000 C spectrophotometer (Thermo Scientific v 1.1). In order to amplify 651 bp fragment from the 5' end of mitochondrial COI gene, PCR reactions were conducted using primer cocktails C_FishF1t1 and C_FishR1t1 as described by Ivanova et al. (2007) and Wong et al. (2011). The amplification reactions were performed in a total volume of 10 [micro]L and included 0.5X Buffer (Promega [R]), 0.2 mM of each deoxynucleotide triphosphate (dNTPs), 2.5 mM MgCh, 0.2 pmol of each primer, 100 ng of genomic DNA, and 1.2 U [micro]L"1 Taq DNA polymerase (Promega[R]). The reactions were conducted using an MJ Research 3130 Thermal Cycler under the following conditions: an initial denaturation at 95[degrees]C for 2 min; 35 cycles of 95[degrees]C for 30 s, 52[degrees]C for 40 s and 72[degrees]C for 1 min; and concluded with a final elongation step of 72[degrees]C for 10 min followed by a hold at 4[degrees]C. Amplified PCR products were subsequently cleaned by the Exo-SAP method (Dugan et al., 2002); 1 [micro]L of PCR product and 0.5 [micro]L EXO SAP-IT (Affymetrix) were incubated for 15 min at 37[degrees]C and 80[degrees]C for 15 min. Thereafter, 1 [micro]L of each purified PCR product was labeled using the BigDye Terminator v 3.1 Cycle Sequencing Kit (Applied Biosystems Inc., CA, USA); 4.5 [micro]L of sterile miliQ water, 2.0 [micro]L of BigDye Sequencing Buffer (400 mM Tris-HCl pH 9.0 and 10 mM MgCh), 2.0 [micro]L of Ready Reaction RR-100 and 0.2 pmol Forward Primer F2_t1 for a total reaction mixture of 10 [micro]L. A sequencing reaction program was run as follows: an initial denaturation at 96[degrees]C for 1 min; 25 cycles of 96[degrees]C for 10 s, 50[degrees]C for 05 s and 60[degrees]C for 4 min, followed by a hold at 4[degrees]C. Then, 5 [micro]L were taken from the resulting sequencing reaction and added with 22.5 [micro]L and 5.0 [micro]L SAMTM and BigDyeR XTerminatorTM (Applied Biosystems Inc., CA, USA) solutions respectively, incubated with agitation of 1000 rpm for 30 min at 24[degrees]C, then centrifuged at 10000 for 10 min and supernatant transferred to a 96 well plate and sequenced on an ABI 31306l Genetic Analyzer (Applied Biosystems Inc., CA, USA). Sequences were edited using Chromas Lite v 2.1.1 (Technelysium, Pty Ltd.). Voucher sequences from GenBank, reference sequences from BOLD (Altschul et al., 1990) databases and consensus sequences of each species generated from this study were compared and aligned using the CLUSTALW software on MegAlign Pro (DNASTAR Inc., Madison, WI). Sample identification based on the sequence similarity approach was carried out using two databases; BOLD and GenBank. The highest percent pairwise identity of the consensus sequence from each species blasted (BLASTN) against NCBI were compared to the percent specimen similarity scores of the consensus sequence from each species within the BOLD-IDS (BOLD Identification System) (Ratnasingham & Hebert, 2007). As commonly applied in DNA barcoding, sequence divergences were estimated by the Kimura 2-parameter substitution model and a phylogenetic tree was constructed with MegAling using an improved version of the Neighbor-Joining algorithm of Satou and Nei (Gascuel, 1997). The robustness of the maximum parsimony tree was assessed by performing bootstrapping analysis with 1000 replicates, and gaps removed by complete deletion (Felsenstein, 1985).

Table 1 shows the comprehensive barcoding identification results based on GenBank or BOLD databases. Both databases revealed identity in the range of 96-100% for consensus sequences of three species (Ictalurus punctatus, I. furcatus, and I. lupus). GenBank-based identification for all species yielded an alignment E-value of 0.0.BOLD-IDS results were in agreement with GenBank results in the identification of these species, yielding 100% identity. However, some entrees on FISH-BOLD were marked as "private" and therefore, even when there could be a more reliable match for the target sequence, it cannot be identified at this moment. All domestic samples used for aquaculture were positively identified as I. punctatus (Table 1). Concerning free-living individuals, most samples were also identified as channel catfish, with the exception of two individuals from Pilon and Corona Rivers in Tamaulipas, identified as I. lupus. With respect to commercial fish, only two samples matched I. punctatus COI sequence: a sample from Panuco River, a natural border between the Mexican States Tamaulipas and Veracruz, was identified as channel catfish, same as a fish purchased from a random fish market located on the center of the State of Tamaulipas. At that same location, another specimen was identified as I. lupus. A fish collected at Chapala Lake, in the State of Jalisco was also identified as I. lupus. Another related species, I. furcatus was found at Champayan Lagoon, located southern state in Tamaulipas.

Identification of channel catfish species in Mexico has several connotations. First of all, it can be inferred that, in spite of the lack of attention that has been given to the species production, aquaculture is based on I. punctatus and not misleading species. An accurate and reliable identification of channel catfish provides a powerful tool for further market analysis of fish products and sub-products. It has been established that almost 25% of fish products in the United States are mislabeled (Wong & Hanner, 2008); most products are intentionally sold as more expensive species. Channel catfish, in particular, has faced great competition against bassa fish (Pangasius spp.) since it is produced at a much lower cost. However, the low-quality requirements of bassa fish make it a potential hazard to health and unfair competition for the channel catfish industry. In the present report, it was observed that when looking for "catfish", different species are available on fish markets. I. lupus and I. furcatus were presented as alternatives for channel catfish consumption but are likely dueto the local availability of fish or a lack of awareness from the consumers. The appropriate identification of species constitutes one of the main concerns regarding population management, such as biodiversity monitoring (Groves et al., 2002; Hajibabaei et al., 2007), recognition of mating and migratory behaviors (Sawyer et al., 2009), and population genetics by providing signals of the extent and nature of population divergences and facilitating comparative studies of population diversity (Taylor et al., 2003; Hebert et al., 2004). Taxonomic identification is usually dependent on the existence of a good quality specimen and the availability of a skilled professional. Molecular identification of wild specimens could be of utmost importance for the study of wild populations. Not only in the present it was possible to verify the reported distribution of Ictalurus species in Mexico such as the case of I. furcatus and I. punctatus on Bravo and Panuco rivers (Garcia de Leon et al., 2005), but we can also report the presence of freeliving channel catfish, Ictalurus punctatus, on eight novel locations within Mexican territory: "Gustavo Diaz Ordaz", "Republica Espanola", "Ramiro Caballero", "Vicente Guerrero" and "La Boquilla" reservoirs and Purificacion, Pilon and Corona rivers (Table 2).

On the other hand, I. furcatus, previously reported in Bravo and Yaqui River (Cuvier & Valenciennes, 1829) was now found on Champayan Lagoon, more than 400 km to the south. Moreover, I. lupus, previously reported in Balsas River and Ixtla River (Jordan & Snyder, 1900), was found at 3 novel locations: Pilon River, Corona River, and Chapala Lake. As it can be noted, Ictalurus species have expanded their original range. This can be attributed to the success of a growing industry. However, it should be noted that undocumented introductions, transportation, and releases could have a negative impact on recognized wild catfish populations. Channel catfish is considered as an invasive species on present days (Gonzalez et al., 2014) and any species with a little survival potential could be dangerous on a new ecosystem. Notwithstanding, the channel catfish should be rather seen as a species with a huge productive potential instead of a threat, while new tools emerge to greatly facilitate our understanding and ability to leverage its maximum potential.

The effectiveness of DNA barcoding was ascertained for channel catfish populations in Mexico. It was verified that aquaculture industry uses only the species I. punctatus. A wider distribution range was observed for three Ictalurus species. A total of 12 novel sites are here reported for I. punctatus, I. furcatus and I. lupus. When commercial samples were analyzed, it was found that I. lupus and I. furcatus were sold as generic "catfish", so it is proposed that molecular identification by DNA barcoding represents a powerful tool in the study of catfish populations and subproducts.

DOI: 10.3856/vol46-issue2-fulltext-23

ACKNOWLEDGMENTS

The first author would like to thank the Mexican Consejo Nacional de Ciencia y Tecnologia (CONACyT) and Instituto Politecnico Nacional (IPN) for scholarships awarded. Special thanks to Pascuala Ambriz for the technical support and everyone involved in sample collection. The present work was supported by 1) Fondo Mixto de Fomento a la Investigacion Cientifica y Tecnologica CONACyT-Gobierno de Tamaulipas. Project number: 150598. 2) Secretaria de Investigacion y Posgrado del Instituto Politecnico Nacional, Mexico. SIP project: 20143982.

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Received: 6 December 2016; Accepted: 17 November 2017

Ana Laura Lara-Rivera (1), Gaspar Manuel Parra-Bracamonte (2) & Xochitl Fabiola De la Rosa-Reyna (2,3)

(1) Instituto de Ciencias Agricolas, Universidad Autonoma de Baja California, Baja California, Mexico

(2) Centro de Biotecnologia Genomica, Instituto Politecnico Nacional, Reynosa, Tamaulipas, Mexico

(3) Department of Wildlife and Fisheries Sciences, Texas A&M University, Texas, USA

Corresponding Author: Gaspar Parra-Bracamonte (pabraman@hotmail.com; gparra@ipn.mx)

Corresponding editor: Leonardo Abitia
Table 1. Sample ID, collection site, location types and
BLASTN results showing species identity, and accession
number. * Blast performed only on FishBol Database and
therefore, no further information of alignments is available.

Sample                                           Location
ID                 Collection site                 type

1150     Purificacion River, Tamaulipas            River
1151     Purificacion River, Tamaulipas
1152     Purificacion River, Tamaulipas
1153     Purificacion River, Tamaulipas
1154     Purificacion River, Tamaulipas
1155     Purificacion River, Tamaulipas
1157     Purificacion River, Tamaulipas
COX17    Purificacion River, Tamaulipas
COX18    Purificacion River, Tamaulipas
COX19    Purificacion River, Tamaulipas
COX20    Purificacion River, Tamaulipas
1173     Pilon River, Tamaulipas
1174     Pilon River, Tamaulipas
1176     Pilon River, Tamaulipas
1177     Pilon River, Tamaulipas
1178     Pilon River, Tamaulipas
1179     Pilon River, Tamaulipas
COX14    Pilon River, Tamaulipas
COX15    Pilon River, Tamaulipas
COX16    Pilon River, Tamaulipas
1231     Corona River, Tamaulipas
1231     Corona River, Tamaulipas
1203     Corona River, Tamaulipas
1202     Corona River, Tamaulipas
1205     Corona River, Tamaulipas
1206     Corona River, Tamaulipas
1207     Corona River, Tamaulipas
1209     Corona River, Tamaulipas
1210     Corona River, Tamaulipas
1533     Bravo River, Tamaulipas
1532     Bravo River, Tamaulipas
1580     Bravo River, Tamaulipas
1530     Bravo River, Tamaulipas
1505     Bravo River, Tamaulipas
1529     Bravo River, Tamaulipas
1535     Bravo River, Tamaulipas
1509     Bravo River, Tamaulipas
PAN13    Panuco River, Veracruz and
           Tamaulipas borderline

1096     Gustavo Diaz Ordaz Dam, Sinaloa         Reservoir
1104     Gustavo Diaz Ordaz Dam, Sinaloa
1109     Gustavo Diaz Ordaz Dam, Sinaloa
1132     Gustavo Diaz Ordaz Dam, Sinaloa
1137     Gustavo Diaz Ordaz Dam, Sinaloa
1139     Gustavo Diaz Ordaz Dam, Sinaloa
1092     Gustavo Diaz Ordaz Dam, Sinaloa
1233     Ramiro Caballero Dam, Tamaulipas
1234     Ramiro Caballero Dam, Tamaulipas
1235     Ramiro Caballero Dam, Tamaulipas
1236     Ramiro Caballero Dam, Tamaulipas
1298     Ramiro Caballero Dam, Tamaulipas
1299     Ramiro Caballero Dam, Tamaulipas
1240     Ramiro Caballero Dam, Tamaulipas
1241     Ramiro Caballero Dam, Tamaulipas
1250     Republica Espanola Dam, Tamaulipas
1251     Republica Espanola Dam, Tamaulipas
1252     Republica Espanola Dam, Tamaulipas
1253     Republica Espanola Dam, Tamaulipas
1254     Republica Espanola Dam, Tamaulipas
1255     Republica Espanola Dam, Tamaulipas
1256     Republica Espanola Dam, Tamaulipas
1257     Republica Espanola Dam, Tamaulipas
1063     Vicente Guerrero Dam, Tamaulipas
1064     Vicente Guerrero Dam, Tamaulipas
1065     Vicente Guerrero Dam, Tamaulipas
1450     La Boquilla Dam, Chihuahua
1451     La Boquilla Dam, Chihuahua
1452     La Boquilla Dam, Chihuahua
1455     La Boquilla Dam, Chihuahua
1457     La Boquilla Dam, Chihuahua
1458     La Boquilla Dam, Chihuahua
1461     La Boquilla Dam, Chihuahua
1459     La Boquilla Dam, Chihuahua

764      Sayula, Jalisco                           Farm
788      Sayula, Jalisco
868      Brisenas, Michoacan
874      Brisenas, Michoacan
995      Villagran, Zacatecas
990      Villagran, Zacatecas
1413     San Fco. de Conchos, Chihuahua
1422     San Fco. de Conchos, Chihuahua
937      General Cepeda, Coahuila
939      General Cepeda, Coahuila
8        "La Dona", Tamaulipas
588      "Aquaque", Tamaulipas
117      "Aquaque", Tamaulipas
75       "La Isla", Tamaulipas
1049     Nuevo Padilla, Tamaulipas              Fish Market
1043     Nuevo Padilla, Tamaulipas              Fish Market
COX6     Champayan, Tamaulipas                  Fish Market
                                               (From Lagoon)
867      Chapala, Jalisco                       Fish Market
                                                (From Lake)
SL1      San Luis Missouri, USA                  Reference
SL3      San Luis Missouri, USA                  from Farm

Sample                         Identity   Max.    Coverage
ID             Species           (%)      score     (%)      E-value

1150        I. punctatus         100      1203       95         0
1151        I. punctatus          91       811       51         0
1152        I. punctatus          99      1173       52         0
1153        I. punctatus          93       79        12       8e-11
1154        I. punctatus          88       374       31       2e-99
1155        I. punctatus          99      1181       94         0
1157        I. punctatus         100      1203       92         0
COX17       I. punctatus          99      1151       90         0
COX18       I. punctatus          98      1053       86         0
COX19       I. punctatus          99      1122       91         0
COX20       I. punctatus          99       736       89         0
1173        I. punctatus          99      1197       92         0
1174        I. punctatus         100      1203       81         0
1176        I. punctatus          99      1219       87         0
1177        I. punctatus          99      1205       87         0
1178       Ictalurus lupus        98      1140       92         0
1179        I. punctatus          99      1214       64         0
COX14       I. punctatus          99      1072       87         0
COX15       I. punctatus          99      1107       88         0
COX16       I. punctatus          99      1077       85         0
1231       Ictalurus lupus        98      1094       96         0
1231       Ictalurus lupus        98      1138       93         0
1203        I. punctatus         100      1203       95         0
1202        I. punctatus         100      11.03      92         0
1205        I. punctatus          99      1182       91         0
1206        I. punctatus          99      1142       93         0
1207        I. punctatus          99      1098       91         0
1209        I. punctatus          99      1035       92         0
1210        I. punctatus          92       981       92         0
1533        I. punctatus          99      1219       96         0
1532        I. punctatus          99       987       77         0
1580        I. punctatus          99      1240       61         0
1530        I. punctatus          99      1219       96         0
1505        I. punctatus          99      1219       96         0
1529        I. punctatus          99      1214       96         0
1535        I. punctatus          99      1208       96         0
1509        I. punctatus          99      1214       96         0
PAN13       I. punctatus          87

1096        I. punctatus          89       795       82         0
1104        I. punctatus          89       852       57         0
1109        I. punctatus         100      1131       57         0
1132        I. punctatus          94      1020       58         0
1137        I. punctatus          86       610       48      1e-170
1139        I. punctatus         100      1208       65         0
1092        I. punctatus          99      1177       97         0
1233        I. punctatus          98       828       98         0
1234        I. punctatus          99       929       90         0
1235        I. punctatus          99      1216       96         0
1236        I. punctatus          99      1099       87         0
1298        I. punctatus          94       922       61         0
1299        I. punctatus         100      1203       92         0
1240        I. punctatus          99      1171       91         0
1241        I. punctatus          99      1214       98         0
1250        I. punctatus         100      1221       93         0
1251        I. punctatus         100      1203       93         0
1252        I. punctatus         100      1214       96         0
1253        I. punctatus         100      1203       93         0
1254        I. punctatus         100      1225       96         0
1255        I. punctatus         100      1203       93         0
1256        I. punctatus         100      1203       93         0
1257        I. punctatus         100      1203       93         0
1063        I. punctatus          99      1162       94         0
1064        I. punctatus          99      1229       97         0
1065        I. punctatus          99      1225       96         0
1450        I. punctatus         100      1219       98         0
1451        I. punctatus          99      1201       96         0
1452        I. punctatus          99      1216       96         0
1455        I. punctatus          99      1197       96         0
1457        I. punctatus         100      1203       92         0
1458        I. punctatus          99      1227       96         0
1461        I. punctatus          99      1219       96         0
1459        I. punctatus         100      1203       93         0

764         I. punctatus          99      1147       89         0
788         I. punctatus          99      1227       97         0
868         I. punctatus         100      1225       96         0
874         I. punctatus         100      1225       97         0
995         I. punctatus         100      1221       97         0
990         I. punctatus         100      1225       96         0
1413        I. punctatus         100      1227       96         0
1422        I. punctatus         100      1203       96         0
937         I. punctatus          99      1221       96         0
939         I. punctatus         100      1203       93         0
8           I. punctatus          94       647       59         0
588         I. punctatus         100       928       91         0
117         I. punctatus         100
75          I. punctatus         100      1227       96         0
1049       Ictalurus lupus        98      1066       87         0
1043        I. punctatus          98      1059       86         0
COX6     Ictalurus furcatus       94       985       88         0
867        Ictalurus lupus        98      1116       95         0
           Ictalurus lupus        97      1064       92         0
SL1         I. punctatus          99       813       90         0
SL3         I. punctatus         100      1203       96         0

Sample      Accession
ID            number

1150        JF292380.1
1151        HQ024943.1
1152        JF292354.1
1153        KF558290.1
1154        EU524678.1
1155        AF482987.1
1157        JF292392.1
COX17       JF292353.1
COX18       JF292353.1
COX19       JF292353.1
COX20       JF292353.1
1173        JF292353.1
1174        JF292380.1
1176        AF482987.1
1177        AF482987.1
1178        JN026911.1
1179        AF482987.1
COX14       JF292353.1
COX15       JF292353.1
COX16       JF292353.1
1231        JN026910.1
1231        JN026911.1
1203        JF292380.1
1202        JF292353.1
1205        JF292386.1
1206        JF292353.1
1207        JF292354.1
1209        JF292353.1
1210        JF292360.1
1533        AF482987.1
1532        JF292353.1
1580        AF482987.1
1530        AF482987.1
1505        AF482987.1
1529        AF482987.1
1535        AF482987.1
1509        AF482987.1
PAN13      * BCFB131-06

1096        JF292392.1
1104        AF482987.1
1109        JF292353.1
1132        JF292387.1
1137        JF292388.1
1139        HQ024943.1
1092        JF292392.1
1233        HQ024943.1
1234        JF292362.1
1235        AF482987.1
1236        JF292353.1
1298        JF292392.1
1299        JF292392.1
1240        JF292392.1
1241        AF482987.1
1250        JF292380.1
1251        JF292392.1
1252        AF482987.1
1253        JF292392.1
1254        AF482987.1
1255        JF292392.1
1256        JF292392.1
1257        JF292392.1
1063        JF292353.1
1064        AF482987.1
1065        AF482987.1
1450        AF482987.1
1451        AF482987.1
1452        AF482987.1
1455        AF482987.1
1457        JF292392.1
1458        AF482987.1
1461        AF482987.1
1459        JF292392.1

764         JF292392.1
788         AF482987.1
868         AF482987.1
874         AF482987.1
995         AF482987.1
990         AF482987.1
1413        AF482987.1
1422        AF482987.1
937         AF482987.1
939         JF292392.1
8           KF558290.1
588         BCFB131-06
117       * ANGBF8222-12
75          AF482987.1
1049        JN026911.1
1043        JF292353.1
COX6        JF292369.1
867         JN026911.1
            JN026910.1
SL1         JF292392.1
SL3         AF482987.1

Table 2. Ictalurus punctatus previous and current distribution.

                                            Present distribution
Previously reported distribution          (as found in this study)

* Balsas River (Mejia et al., 2013).
* Rio Bravo Hydrological System.
The "Rio Bravo" Hydrological system
  includes Salado River, Alamo
  River, San Juan
River, Bravo River, Anzalduaz Dam,
  Retamal Dam and Madre Lagoon.
* San Fernando Hydrological System           Purificacion River
"San Fernando" Hydrological System               Pilon River
  includes San Fernando, Potosi and
  Linares rivers.
* Soto La Marina Hydrological System            Corona River
"Soto La Marina" Hydrological                    Bravo River
  System is constituted by Soto La              Panuco River
  Marina, San Carlos, Pilon,             Vicente Guerrero Reservoir
  Purificacion, Corona, San Felipe,
  Santa Ana, San Marcos and
  Arroyo Grande rivers.
* Guayalejo-Tamesi Hydrological         Republica Espanola Reservoir
  System (Page & Burr, 1991;
  Perez-Ponce & Choudhury, 2002).
The "Guayalejo-Tamesi" Hydrological          Gustavo Diaz Ordaz
  system includes Hieu, Nogales,            Reservoir La Boquilla
  San Vicente, Jaumave, Guayalejo,                Reservoir
  Sabinas, Frio, Las Flores,
  Mante, Tigre and Tamesi rivers.
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Title Annotation:Short Communication
Author:Lara-Rivera, Ana Laura; Parra-Bracamonte, Gaspar Manuel; De la Rosa-Reyna, Xochitl Fabiola
Publication:Latin American Journal of Aquatic Research
Date:May 1, 2018
Words:4532
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