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Open AccessArticle

Ichthyological Differentiation and Homogenization in the Pánuco Basin, Mexico

1
Centro de Investigación en Biodiversidad y Conservación, Universidad Autónoma del Estado de Morelos, Cuernavaca, Morelos 62209, Mexico
2
Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo, Pachuca, Hidalgo 42001, Mexico
3
Departamento de Sistemática y Ecología Acuática, El Colegio de la Frontera Sur, Chetumal, Quintana Roo 77010, Mexico
4
Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Morelos, Cuernavaca, Morelos 62209, Mexico
5
Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional, Unidad Oaxaca, Instituto Politécnico Nacional, Santa Cruz Xococotlán, Oaxaca 71230, Mexico
*
Author to whom correspondence should be addressed.
Diversity 2020, 12(5), 187; https://doi.org/10.3390/d12050187
Received: 10 April 2020 / Revised: 1 May 2020 / Accepted: 5 May 2020 / Published: 11 May 2020
(This article belongs to the Special Issue Effects of Human Disturbance on Ecological Communities)

Abstract

Species introductions and extirpations are key aspects of aquatic ecosystem change that need to be examined at large geographic and temporal scales. The Pánuco Basin (Eastern Mexico) has high ichthyological diversity and ecological heterogeneity. However, freshwater fish (FWF) introductions and extirpations since the mid-1900s have modified species range and distribution. We examine changes in FWF species composition in and among four sub-basins of the Pánuco by comparing fish collection records pre-1980 to 2018. Currently, the FWF of the Pánuco includes 95 species. Fishes in the Poeciliidae, Cyprinidae, and Cichlidae, respectively, comprised most records over time. Significant differences in species composition were found between the first (pre-1980) and last (2011–2018) study periods, but not for periods in-between. Eight independent species groups were key for explaining changes in Pánuco river ichthyofauna; one group was dominated by invasive species, and saw increases in the number of records across study periods (faunal homogenization). Another group was formed by species with conservation concern with a declining number of records over time. Thirteen (2 native and 11 non-native) species were responsible for temporal turnover. These results strongly suggest high rates of differentiation over time (via native species loss) following widespread non-native species introductions.
Keywords: biogeography; community composition; differentiation; freshwater fishes; homogenization; Pánuco basin; watershed biogeography; community composition; differentiation; freshwater fishes; homogenization; Pánuco basin; watershed

1. Introduction

Rapid ecosystem and species loss results from pollution, as well as land use and climate change [1]. Human activity does not solely lead to species loss; it can also lead to increases in faunal similarity by the alteration of species range [2] via species introductions and species loss. Anthropogenic introductions expand a species´ range beyond its natural dispersal capacity; species loss can result from human driven ecosystem and habitat deterioration [2,3,4,5]. The number and manner of species loss and introductions occurring can result in different levels of biological homogenization and differentiation [5,6]. Lacking extirpations, the introduction of a given invasive in two sites leads to an increase in their similarity. Alternatively, the introduction of different invasive species in two sites will reduce among-site similarity [5]. Loss of species shared among two sites will also generate biological differentiation [5,7]. Human-caused biological homogenization and differentiation are serious threats to global biodiversity [8,9,10]. Trends in both biological homogenization and differentiation can be used as tools for the development of conservation strategies [7]. Processes of homogenization and differentiation have been documented for freshwater fish faunas in North America and Europe [8,9,10,11]. Generally, studies have found increasing rates of among-region homogenization caused primarily by non-native species introductions and translocations, as well as urbanization, but also loss of community similarity driven by non-native species in certain settings [10]. While the expansion and disappearance of non-native and native species, respectively, have been the focus of an increasing body of literature in Latin America [12,13,14], processes of homogenization or differentiation have not been formally addressed in published literature in Mexico. Understanding the rates and causes of homogenization and differentiation in this species-rich area of the world could help identify strategies to help in conservation efforts of unique faunas. As a first step in understanding whether and how these processes are happening in the freshwater fish fauna of the Pánuco Basin, here, we examine their rates in one of the most important basins of Mexico.
The Pánuco Basin is one of the largest (9.7 million ha) and most diverse in the Mexican Gulf of Mexico slope [15]. Nearctic and Neotropical freshwater fish (FWF) faunas converge in this basin, which is also a transition zone between three Mexican physiographic regions [16,17]. A complex geology has led to a relatively high proportion (57%) of FWF in Mexico being endemic or microendemic [18]. Approximately 95 (native and non-native) species have been recorded in the basin [19] from a variety of sources, including species lists and inventories, and conservation-oriented studies [17,20,21,22]. Some studies have provided evidence on the impacts of introduced species on natives such as Cualac tessellatus, Ataeniobius toweri, Tampichthys mandibularis, and T. dichroma [21,23] in the Pánuco. However, homogenization and differentiation processes have not been addressed for the basin. The analysis of these processes can shed light on the temporal dynamics and causes that have led to the current distribution of species in the Pánuco. Here, we explore and quantify FWF homogenization and differentiation processes for four sub-basins in the Pánuco based on fish collections and museum information spanning more than 50 years of data. We hypothesize a temporal increase in FWF homogenization and then differentiation for the entire Pánuco, as well as among the four sub-basins.

2. Materials and Methods

2.1. Units of Analysis

The Pánuco basin spans a large (97,196 km2), ecologically and geographically diverse area. The mainstem of the Pánuco runs generally SW–NE for 510 km from its source to the Gulf of Mexico [24]. The Pánuco runs from the central Mexican plateau and the Sierra Madre Oriental, along rugged terrain to reach a relatively short coastal plateau. It drains the states of Tamaulipas, San Luis Potosí, Hidalgo, Querétaro, México, Guanajuato, and Veracruz [7] (Figure 1). As classified by the Mexican Institute for Geography and Statistics (INEGI), the National Institute of Ecology (INE) and the National Water Commission (CONAGUA), the Pánuco includes four sub-basins :(A) Río Pánuco, (B) Río Tamesí, (C) Río Tamuín, and (D) Río Moctezuma [25] (Figure 1). The Río Pánuco sub-basin is in the states of Tamaulipas and Veracruz [16]; it is the lowest portion of the Pánuco Basin and is comprised of the outlet of the San Juan and Tula rivers downstream from the Zimapán Dam on the Moctezuma and the confluence of the Tamuín River. The Rio Tamesí (originates with the name of Guayalejo river) sub-basin flows NW–SE in the states of Tamaulipas, San Luis Potosí, and Veracruz [7,24]. The Río Tamuín starts in the state of San Luis Potosí after the confluence of the Verde and Santa María rivers, and includes the Gallinas, Tamasopo, El Salto, and Valles rivers. The Calabazas and Los Hules rivers are also located in this sub-basin. The Moctezuma sub-basin includes the San Juan, Extoraz (Tolimán and Victoria), Amajac, and Tempoal rivers and drains the states of Hidalgo, Querétaro, México, San Luis Potosí, Guanajuato, and Veracruz [7]. Administratively, this sub-basin includes the once endorheic Mexico City valley as part of the Moctezuma; this valley has not been included in our study.
The above sub-basins were used as geographical units of analysis upon which we studied homogenization and differentiation processes. That is, FWF changes though time were analyzed in each sub-basin and contrasted with those of other sub-basins.

2.2. Database

Sub-basin specific databases were constructed using historical (pre-1980 to 2018) FWF collection information. The presence of only primary and secondary species (FWF with little or no tolerance to ocean salinity) [26] collected in sites located in each of the Pánuco sub-basins was included in the database. Databases were populated primarily from data in FISHNET2 [27] and the Global Biodiversity Information Facility [28]. Both repositories were searched using Pánuco and Panuco as geographic keywords to locate records for the river basin. GBIF data included a 2018 update from the Colección Nacional de Peces Dulceacuícolas Mexicanos de la Escuela Nacional de Ciencias Biológicas [19]. The geographic location for each record found in databases was verified using QGIS 3.8 and adjusted, when necessary, to fall within each sub-basin. Fish records from Miller et al. (2009) [15], from the “Edmundo Díaz Pardo” fish collection at the Universidad Autónoma de Querétaro, were also obtained and their coordinates were revised. Additionally, the Web of Science (Clarivate Analytics©, Philadelphia, PA, USA.) was searched for recent (up to 18 years prior to 2018) publications reporting on Pánuco river collections or other ichthyological studies [29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62]. Species and genera names in each collection or source were verified and updated [63,64] to adjust synonymy and eliminate possible misidentifications.
Using its date, each collection was assigned to one of five time intervals. Interval 1 included pre-1980 (including 1980) records; interval 2 included records from between 1981 and 1990; and intervals 3, 4, and 5 spanned 1991–2000, 2001–2010, and 2011–2018, respectively.
Thus, the resulting database had presence-absence (0,1) data for each species, an identifier for the sub-basin where it was collected (A, B, C, D) and the time interval (1–5) when it was recorded. These data were used to carry out similarity analyses described below.
We defined species native to the Pánuco as those whose original distribution included a waterbody in the Pánuco. Any species with natural range outside the Pánuco was regarded as non-native. Among these, invasive species were defined based on the categorization by the Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO), which defines invasive species for Mexico [65].

2.3. Analyses

We first estimated sample completeness [66], using species accumulation curves (bootstrap) from all intervals with EstimateS [67]. We then quantified biological homogenization or differentiation between sub-basins and among time intervals. We used Jaccard´s similarity index to calculate distance matrices among species and time intervals, and among sub-basins using PERMANOVA (permutational multivariate analysis of variance) [68,69]. Next, we carried out a pairwise comparison among intervals and sub-basins, graphically displaying Jaccard values via a boostrapped MDS (multidimensional scaling) procedure among intervals and sub-basins. PERMANOVA and MDS were performed in Primer 7 [70]. Subsequently, we carried out a dual cluster analysis to identify species associations throughout the Pánuco, based on the time interval and the sub-basin where they were found. To achieve this, we converted presence-absence (0,1) data into ordinal data (i.e., the number of sub-basins in which a species is present per time interval) and used Ward´s method for calculating Euclidean distances among time-intervals and sub-basins [71] in Past3 [72].
To identify species responsible for among sub-basin and time-period differences, we carried out four generalized discriminant analyses (GDA). Two (one for sub-basin differences and one for time-period differences) included all 95 species; they identified 15 species with the highest correlations. Two more GDAs (one for sub-basin differences and one for time-period differences) were carried out using only these 15 species. These analyses were carried out in software Statistica v.10 [73].

3. Results

Our database included 95 species in 35 genera, 12 families, and 10 orders (Figure 1). Families with the most species were Poeciliidae (34.7%), Cyprinidae (20%), and Cichlidae (15.8%) (Table A1 and Table A2). Species accumulation curves for all intervals resulted in 94.79% of estimated richness. For each interval, independently, species accumulation curves represented >80% of estimated richness.
Significant differences in species composition were detected among the oldest and most recent time intervals according to pairwise comparison procedures (t = 1.5705, p = 0.022; Figure 2a); however, no differences were found among other time intervals. Species composition differed among all sub-basins (Fpseudo = 9.2383, df = 3, p = 0.001; Figure 2b). The Río Pánuco and the Río Tamuín sub-basins shared the least species (24%) when all time intervals were considered. The Río Moctezuma and Río Tamuín sub-basins shared the most (55%) species. When comparing among intervals, intervals 2 and 3 (1981–1990 and 1990–2000, respectively) shared 91% of species. Intervals 1 and 5 (pre-1980 and 2011-2018, respectively) shared the least species (44%).
Dual grouping analyses resulted in eight distinct groups. Group 1 had species found in more than two sub-basins in the first four intervals and whose presence in the last interval declined. Group 2 was formed by species present in more than three sub-basins in the first three time intervals and then declined after the fourth time interval. Fish species in group 3 were rare in the first intervals and were found in more than three sub-basins by the fourth and fifth time intervals. All fish species in group 4 were present in more than three sub-basins in all intervals. Group 5 was formed by species exclusive to each sub-basin, which were present in the first three intervals, but absent in the last one. Fishes in group 6 were present throughout all time intervals. Group 7 was formed by fish species present in the last three intervals only. Finally, group 8 included species recorded in time interval 1, but absent thereafter (Figure 3; Table 1).
The GDA analysis for time intervals explained 97.89% of the variation with two discriminant functions, DF1 (first discriminant function) 92.79% and DF2 (second discriminant function) 5.1%. The species that most contributed to the over time-species changes were Algansea tincella, Amatitlania nigrofasciata, Ataeniobius toweri, Carassius auratus, Chirostoma grandocule, Coptodon rendalli, C. zillii, Ctenopharyngodon idella, Cyprinus carpio, Gambusia affinis, G. marshi, Ictiobus bubalus, and Notropis boucardi (Table 2). For the sub-basin GDA analysis, we found 97.38% of the variation explained by two functions (DF1: 87.67% and DF2: 9.71%), highly correlated to the presence of A. tincella, A. nigrofasciata, A. toweri, C. auratus, C. grandocule, C. rendalli, C. zillii, C. idella, C. carpio, G. marshi, Gambusia atrora, G. panuco, I. bubalus, and N. boucardi (Table 3).

4. Discussion

4.1. Compositional Changes

Our study discovered differentiating trends in FWF fauna of the Pánuco River over the last 50 years. While significant differences were found only between the first and last interval, changes occurred gradually over our study period. The first and second time intervals shared 82% of species, with 15 species recorded in time period 1 being lost in interval 2. These included 12 non-native species (i.e., invasive C. zilli [65]), which were perhaps unable to become established, and three native species (i.e., critically endangered Notropis calientis [74]). Between time intervals 2 and 3, Pánuco sub-basins were more homogenous (similarity at 91%), and six non-native species were introduced (including invasives A. nigrofasciata, Oncorhynchus mykiss, and O. niloticus, [65]). Native species like Xiphophorus continens (data deficient according to [75]) were not found after the third time interval. Interestingly, species homogenization was only found in these first three time intervals, coinciding with a nation-wide policy for species introductions for aquaculture. During the 1970s and 1980s, several governmental programs promoted fish farms and planting of non-natives in newly created reservoirs [76]. These policies led to a substantial increase in the number of introduced species throughout the country [23,77,78]. Past these time intervals, we noted a decline in species similarity, which has continued to the present. The third and fourth intervals shared 86% of species, but four non-natives (including invasives Hypophthalmichthys molitrix and C. idella [65]) were first found in the Pánuco. Seven species, including Herichthys pame, Xiphophorus nigrensis, and Tampichthys rasconis (this last one being endangered [79]) were not found after interval 4. The highest differentiation (59% of species shared) was found between intervals 4 and 5, with 29% of species in period 4 not found in period 5, and two newly introduced species.
Gradual differentiation over time ultimately resulted in only 34% of species being shared between the first and last time intervals. This included 47% of species registered in the first time interval not being recorded in the latest time intervals and the introduction of 10% of nonnative species, of which 50% are considered invasive [65]. While we expected continually increasing homogenization over time in the Pánuco basin, what we detected was a marked increase in ichthyological differentiation (vía species loss) occurring after non-natives had been introduced in the region. Several studies have demonstrated that species invasions can result in native species loss [80,81,82]. Nile perch (Lates niloticus) introductions into Lake Victoria (Africa) [83] and loricariid introductions into Infiernillo Reservoir in Mexico [84,85] are examples of how invasives have led to collapses of native faunas. There are, however, many instances in which it is difficult to establish a cause and effect relationship between a species introduction and the demise of native species. For example, the introduction of Oreochromis mossambicus in the State of Morelos in the 1970s coincided with the local extirpation of Poeciliopsis balsas. While the effects of the non-native species were cited as a likely cause for the extirpation [77,86], the mechanism leading to the disappearance of the native species was not clearly established. Similar to this study, in our analysis, we identified increases in the distribution of non-natives broadly coinciding with diminishing records for native species.

4.2. Assemblage Change among Time Intervals

Our cluster analyses helped us identify which species entered or were lost from sub-basins through time. Group 3 was integrated by invasive species that expanded their range after being introduced into one of the sub-basins. Group 7, also integrated by non-native species, was composed of species that did not appear in later time intervals, suggesting they were not able to become established. These two groups include 17% of all species found in the Pánuco Basin, and are species highly utilized in aquaculture, commercial and sport fisheries, and for biocontrol worldwide [78,86,87]. Groups 1 and 5 were mostly composed of species under conservation status and that were not found in later time intervals. These can be considered the most vulnerable groups and comprise 40% of species of the Pánuco. These groups include Herichthys steindachneri, A. toweri, Herichthys bartoni, Notropis calabazas, T. mandibularis, T. rasconis, and Xenoophorus captivus, all of which are listed by the International Union for Conservation of Nature (IUCN) and NOM 059 SEMARNAT 2010 as critically endangered or threatened. Future expeditions to sites where they were previously collected should focus on searching for these species.
Two large groups formed in our analyses. One included non-native, invasive species whose ecological plasticity and life history traits (i.e., adaptability, high reproductive output, and dispersal capacity) allowed their expansion throughout the basin, potentially leading to negative interactions (i.e., interference, predation, and competition) with native species [88]. A second group was formed by native species, many of which are known from unique, often isolated, freshwater ecosystems (i.e., desert springs or small headwater streams) or have relatively small ranges (i.e., Notropis calabazas, Xiphophorus pygmaeus, X. nigrensis). Native faunas are generally vulnerable to the introduction of competitors and predators, in addition to being susceptible to disease [89]. That many native species were not registered in our latest time intervals suggests accelerated species loss. This needs to be addressed by the implementation of species-specific conservation measures. We acknowledge that our work is limited by a lack of concise information on species absence in databases, which prevents us from calculating the actual number of species disappearing in the Pánuco. However, 37% of species not found in the last time interval of our analysis are also listed by IUCN or NOM-059-SEMARNAT-2010, and another 35% are considered data-deficient by IUCN. Our study points to a potentially accelerated rate of species loss from a regional perspective. Further, we recognize that our datasets may be affected by differences in sampling efforts carried out over time. Our dataset results from the efforts from many scientists across decades whose sampling goals, strategies, and methods may have differed considerably. Large-scale studies that integrate information from a variety of sources are subject to such biases in sampling methodology [90,91,92]. Despite these limitations, we feel our use of rarefaction curves and relatively long time periods for analysis help address some of the issues derived from a lack of standardization [93].

4.3. Species Contribution

We identified 13 species generating significant changes across time intervals. Two were native and eleven (including five invasives) were non-native. Cyprinids Cyprinus carpio, C. idella, and C. auratus were introduced prior to the 1980s for use in aquaculture and aquariums and are today well established in the Pánuco and generally throughout the country [15,85]. Cichlids A. nigrofasciata and C. zilli, also non-natives causing significant changes in across time intervals, are known for negatively affecting native cichlids and cyprinids [94,95,96]. Fourteen species were responsible for differences among sub-basins. Most of the species responsible for changes in among time-interval differences were also involved in among sub-basin differences. Only Gambusia panuco and G. atrora were responsible for among sub-basin differences, but not for among time interval differences. These results strongly suggest that non-native, invasive species of use in aquaculture could be largely responsible for changes in the fish composition of the Pánuco Basin. Local and federal programs for fomenting aquaculture will continue to be implemented in the country, leading to increased non-native species introductions [97] and affecting native fish communities [85]. Further threats include dewatering of many streams and rivers and pollution. For example, water irrigation districts such as Mante, Xocoténcatl, and Río Pánuco, Las Ánimas modify water courses and deviate steam water to sugar cane, citrus, and other crop plantations [98]. Especially in the upper (San Juan and Tula rivers) and lower (Tampico-Madero and Altamira rivers) Pánuco basin, pollution from agriculture and industry has seriously affected aquatic systems, rendering several river stretches uninhabitable [99]. These activities will continue to affect native faunas unless their operation is modified, taking into consideration needs for protecting natural habitats or via adoption of impact mitigation strategies, especially in areas of high endemism [100]. Our results can be used to identify species that are likely in the most danger of being affected by anthropogenic activities.
While much is known about how non-native species alter freshwater ecosystem structure and function, studies that incorporate a long-term and ample geographic scale perspective can help us understand the magnitude of the challenges imposed by biological homogenization and differentiation [101]. Being the first approximation to quantify fish fauna homogenization and differentiation rates in Mexico, we believe this study offers information and an analytical approach that could be implemented in other areas of the country. Further, it highlights aspects of faunal change that should be incorporated into national and regional strategies for biodiversity conservation.

5. Conclusions

The Pánuco River remains one with high ichthyological diversity despite being subject to numerous anthropogenic alterations over the last 40 years. Arrival of numerous non-native species and disappearance of endemic species has led to increasing ichthyological homogenization and then differentiation among the four sub-basins comprising the Pánuco Basin. Unfortunately, due to a lack of strict and effective conservation efforts, it is likely differentiation trends will continue as consequence of ongoing environmental degradation (primarily through damming and river desiccation). Homogenization might continue to occur as non-native species continue to expand throughout the basin, likely because of species dispersal via aquaculture programs and releases of aquarium species.

Author Contributions

N.M.-L. and N.M.-S. conceived the idea for this study with considerable assistance from J.J.S.-S.; N.M.-L. and G.I.C.-R. collected data; N.M.-S., N.M.-L., and V.S.-D. developed various aspects of the methodology; N.M.-L and A.P.M.-F. carried out various analyses of the data; N.M.-S., N.M.-L., and H.M.-M. wrote, edited, and prepared the manuscript for submission.; All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Acknowledgments

We thank Ramírez-Herrejón J.P. for assistance in obtaining data from the “Edmundo Díaz Pardo” fish collection of the Universidad Autónoma de Querétaro. Octavio-Aguilar P. assisted with analyses. The Consejo Nacional de Ciencia y Tecnología awarded doctoral program support to N.M.-L. in calls-for-proposals no. 291197 and no. 291277. This paper is a product of N.M.-L.´s PhD degree at the Doctorado en Ciencias Naturales of the Universidad Autónoma del Estado de Morelos, Mexico.

Conflicts of Interest

The authors declare no conflict of interest.

Appendix A

Table A1. Freshwater fish species from the Pánuco Basin registered (1 = presence, 0 = absence) in five time intervals and four sub-basins: (A) Río Pánuco, (B) Río Tamesí, (C) Río Tamuín, and (D) Río Moctezuma.
Table A1. Freshwater fish species from the Pánuco Basin registered (1 = presence, 0 = absence) in five time intervals and four sub-basins: (A) Río Pánuco, (B) Río Tamesí, (C) Río Tamuín, and (D) Río Moctezuma.
No.Scientific NameInterval 1 (≤1980)Interval 2 (1981–1990)Interval 3 (1991–2000)Interval 4 (2001–2010)Interval 5 (2011–2018)
ABCDABCDABCDABCDABCD
1Algansea tincella00110011001100110000
2Amatitlania nigrofasciata00000000000100010001
3Astyanax rioverde00100010001000100010
4Astyanax mexicanus11111111111111111111
5Ataeniobius toweri00100010001000100000
6Atractosteus spatula11110000000000000000
7Carassius auratus01010001000100110011
8Chirostoma arge00000000000000000010
9Chirostoma grandocule10010000000000000000
10Chirostoma humboldtianum00010001000100010000
11Chirostoma jordani00010001000100010000
12Coptodon rendalli00010000000000000000
13Coptodon zillii01010000000000000000
14Ctenopharyngodon idella00000000000001100000
15Cualac tessellatus00100010001000100000
16Cyprinella lutrensis01110001000100010000
17Cyprinus carpio00010001000101010111
18Gambusia affinis11110111011101110110
19Gambusia atrora00010001000100011000
20Gambusia aurata01000100010001000000
21Gambusia marshi01000101010010000000
22Gambusia panuco11110111011101100010
23Gambusia quadruncus10110000000000000000
24Gambusia regani11111111111111110011
25Gambusia vittata11111111111111110101
26Girardinichthys multiradiatus00010000000000000000
27Girardinichthys viviparus00010001000100010001
28Goodea atripinnis00110011001100110011
29Goodea gracilis00110011001100110001
30Herichthys bartoni00100010001000100000
31Herichthys carpintis11110011001100100010
32Herichthys cyanoguttatus11111111111111110011
33Herichthys labridens01110111011101110010
34Herichthys molango00010001000100010000
35Herichthys pame00100010001000000000
36Herichthys pantostictus11111111111111110010
37Herichthys steindachneri01100110011001110010
38Herichthys tamasopoensis00100010001000100010
39Hypophthalmichthys molitrix00000000000001000101
40Ictalurus australis01110111011101110000
41Ictalurus furcatus11110100010001000100
42Ictalurus lupus01000000000000000000
43Ictalurus mexicanus01110111011101110010
44Ictalurus punctatus01110101010101010101
45Ictiobus bubalus01000100001000000000
46Ictiobus labiosus11110011001100110010
47Lepisosteus osseus11110001000100010000
48Lepomis macrochirus00010001000100010011
49Micropterus salmoides10111011101111111111
50Notropis aguirrepequenoi01000000000000000000
51Notropis boucardi00000000001000000000
52Notropis calabazas00100010001000100000
53Notropis calientis01100000000000000000
54Notropis sallaei00110001000100010000
55Notropis tropicus01110101010101010000
56Oncorhynchus mykiss00000000001100010001
57Oreochromis aureus00010001001111111111
58Oreochromis mossambicus00010001001101110111
59Oreochromis niloticus00000000001101110111
60Poecilia formosa11111100110011000000
61Poecilia latipinna11000000000000000000
62Poecilia latipunctata01110111011101100000
63Poecilia limantouri01110000000000000000
64Poecilia mexicana11111111111111110011
65Poecilia reticulata00010001000100010001
66Poecilia sphenops01100010001000000000
67Poeciliopsis gracilis01110011001110110010
68Poeciliopsis infans00010000001000100010
69Poeciliopsis lucida00000000001000000000
70Pseudoxiphophorus bimaculatus00010001001100110011
71Pseudoxiphophorus jonesii00110011001100110001
72Pylodictis olivaris00110000000001000000
73Tampichthys catostomops00100010001000100010
74Tampichthys dichroma00100010001000100010
75Tampichthys erimyzonops01110101010101010000
76Tampichthys ipni01110111011101010000
77Tampichthys mandibularis00100010001000100000
78Tampichthys rasconis00100010001000000000
79Thorichthys maculipinnis00000000000000100000
80Xenoophorus captivus00110010001000100000
81Xenotoca variata00110011001100100010
82Xiphophorus birchmanni00010001000110010001
83Xiphophorus continens00100010000000000000
84Xiphophorus cortezi00110011001100110000
85Xiphophorus hellerii00010001000100010000
86Xiphophorus maculatus01000000000000000000
87Xiphophorus malinche00010001000100010001
88Xiphophorus montezumae01110011001000100010
89Xiphophorus multilineatus00100010001000100010
90Xiphophorus nezahualcoyotl01100110011001100000
91Xiphophorus nigrensis00100010001000000000
92Xiphophorus pygmaeus00110001000101010000
93Xiphophorus variatus11111111111111110111
94Xiphophorus xiphidium01000000000000000000
95Yuriria alta00000000000000000010
Table A2. Categories of freshwater fish species from the Pánuco Basin. We include origin for species, N = native to the basin, NN = non native to the basin; if NN, we specify which sub-basin they are NN in (A = Pánuco, B = Tamesí, C = Tamuín, and D = Moctezuma). We also include species categorized as invasive by Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO) and the category for species under the International Union for Conservation of Nature’s Red List of Threatened Species and the Norma Oficial Mexicana NOM 059 SEMARNAT 2010 (see below).
Table A2. Categories of freshwater fish species from the Pánuco Basin. We include origin for species, N = native to the basin, NN = non native to the basin; if NN, we specify which sub-basin they are NN in (A = Pánuco, B = Tamesí, C = Tamuín, and D = Moctezuma). We also include species categorized as invasive by Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO) and the category for species under the International Union for Conservation of Nature’s Red List of Threatened Species and the Norma Oficial Mexicana NOM 059 SEMARNAT 2010 (see below).
No.FamilyScientific NameORIGINInvasive (Yes /No)Red List Iucn Nom 059 Semarnat 2010
(Native = N, Non Native = NN)Sub-Basin
(A,B,C,D)
1CyprinidaeAlgansea tincellaN CNoLCNo
2CichlidaeAmatitlania nigrofasciataNN YesNENo
3CharacidaeAstyanax rioverdeNCNoLCNo
4CharacidaeAstyanax mexicanus *NABCDNoLC/VUNo/A
5GoodeidaeAtaeniobius toweriNCNoENP
6Lepisosteidae Atractosteus spatulaNBNoLCNo
7CyprinidaeCarassius auratusNN YesLCNo
8AtherinopsidaeChirostoma argeNN NoDDNo
9AtherinopsidaeChirostoma grandoculeNN NoDDNo
10AtherinopsidaeChirostoma humboldtianumNN NoNENo
11AtherinopsidaeChirostoma jordaniNN NoLCNo
12CichlidaeCoptodon rendalliNN NoLCNo
13CichlidaeCoptodon zilliiNN YesLCNo
14CyprinidaeCtenopharyngodon idellaNN YesNENo
15CyprinodontidaeCualac tessellatusNCNoVUP
16CyprinidaeCyprinella lutrensisNCNoLCA
17CyprinidaeCyprinus carpioNN YesVUNo
18PoeciliidaeGambusia affinisNN NoLCNo
19PoeciliidaeGambusia atroraNDNoDDNo
20PoeciliidaeGambusia aurataNBNoDDNo
21PoeciliidaeGambusia marshiNN NoLCA
22PoeciliidaeGambusia panucoNABNoDDNo
23PoeciliidaeGambusia quadruncusNACNoNENo
24PoeciliidaeGambusia reganiNABCDNoDDNo
25PoeciliidaeGambusia vittataNBNoLCNo
26GoodeidaeGirardinichthys multiradiatusNN NoENNo
27GoodeidaeGirardinichthys viviparusNN NoENP
28GoodeidaeGoodea atripinnisNCNoLCNo
29GoodeidaeGoodea gracilisNCNoLCNo
30CichlidaeHerichthys bartoniNCNoENP
31CichlidaeHerichthys carpintisNABNoLCNo
32CichlidaeHerichthys cyanoguttatusNN NoLCNo
33CichlidaeHerichthys labridensNBNoENA
34CichlidaeHerichthys molangoNDNoLCNo
35CichlidaeHerichthys pameNCNoNENo
36CichlidaeHerichthys pantostictusNBANoLCNo
37CichlidaeHerichthys steindachneriNCNoENP
38CichlidaeHerichthys tamasopoensisNCNoVUNo
39CyprinidaeHypophthalmichthys molitrixNN YesNTNo
40IctaluridaeIctalurus australisNBNoDDA
41IctaluridaeIctalurus furcatusNCDNoLCNo
42IctaluridaeIctalurus lupusNN NoDDNo
43IctaluridaeIctalurus mexicanusNCNoVUA
44IctaluridaeIctalurus punctatusNBCDNoLCNo
45CatostomidaeIctiobus bubalusNN NoLCA
46CatostomidaeIctiobus labiosusNCDNoDDNo
47LepisosteidaeLepisosteus osseusNABCNoLCNo
48CentrarchidaeLepomis macrochirusNN NoLCNo
49CentrarchidaeMicropterus salmoidesNN YesLCNo
50CyprinidaeNotropis aguirrepequenoiNN NoVUPr
51CyprinidaeNotropis boucardiNN NoENA
52CyprinidaeNotropis calabazasNCNoCRNo
53CyprinidaeNotropis calientisNCNoCRNo
54CyprinidaeNotropis sallaeiNDNoLCNo
55CyprinidaeNotropis tropicusNBCNoNTNo
56SalmonidaeOncorhynchus mykissNN YesNEPr
57CichlidaeOreochromis aureusNN YesLCNo
58CichlidaeOreochromis mossambicusNN YesNTNo
59CichlidaeOreochromis niloticusNN YesLCNo
60PoeciliidaePoecilia formosaNABDNoLCNo
61PoeciliidaePoecilia latipinnaNN NoLCNo
62PoeciliidaePoecilia latipunctataNBNoDDP
63PoeciliidaePoecilia limantouriNN NoNENo
64PoeciliidaePoecilia mexicanaNABCDNoLCNo
65PoeciliidaePoecilia reticulataNN Yes NENo
66PoeciliidaePoecilia sphenopsNN NoLCPr
67PoeciliidaePoeciliopsis gracilisNN NoLCNo
68PoeciliidaePoeciliopsis infansNN NoLCNo
69PoeciliidaePoeciliopsis lucidaNN NoDDNo
70PoeciliidaePseudoxiphophorus bimaculatusNN NoLCNo
71PoeciliidaePseudoxiphophorus jonesiiNN NoLCNo
72IctaluridaePylodictis olivarisNN NoLCNo
73CyprinidaeTampichthys catostomopsNCNoNTNo
74CyprinidaeTampichthys dichromaNCNoNEA
75CyprinidaeTampichthys erimyzonopsNBCNoDDNo
76CyprinidaeTampichthys ipniNBCDNoLCNo
77CyprinidaeTampichthys mandibularisNCNoENP
78CyprinidaeTampichthys rasconisNCNoENNo
79CichlidaeThorichthys maculipinnisNN NoNENo
80GoodeidaeXenoophorus captivusNCNoENP
81GoodeidaeXenotoca variataNCNoLCNo
82PoeciliidaeXiphophorus birchmanniNDNoLCNo
83PoeciliidaeXiphophorus continensNCNoDDNo
84PoeciliidaeXiphophorus corteziNCDNoDDNo
85PoeciliidaeXiphophorus helleriiNN NoLCNo
86PoeciliidaeXiphophorus maculatusNN NoDDNo
87PoeciliidaeXiphophorus malincheNDNoDDNo
88PoeciliidaeXiphophorus montezumaeNCNoDDNo
89PoeciliidaeXiphophorus multilineatusNCNoDDNo
90PoeciliidaeXiphophorus nezahualcoyotlNBCNoDDNo
91PoeciliidaeXiphophorus nigrensisNCNoDDNo
92PoeciliidaeXiphophorus pygmaeusNCNoDDNo
93PoeciliidaeXiphophorus variatusNABCDNoLCNo
94PoeciliidaeXiphophorus xiphidiumNN NoLCNo
95CyprinidaeYuriria altaNN NoENNo
RED LIST IUCN—the International Union for Conservation of Nature’s Red List of Threatened Species: NE = not evaluated; DD = data deficient; LC = least concern; NT = near threatened; VU = vulnerable; EN = endangered; CR = critically endangered. NOM 059 SEMARNAT 2010—NORMA Oficial Mexicana NOM-059-SEMARNAT-2010, Protección ambiental-Especies nativas de México de flora y fauna silvestres-Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio-Lista de especies en riesgo: No = not in the NOM; Pr = subject to special protection; A = amenazadas (threatened); P = en peligro de extinción (in danger of extinction).* For A. mexicanus, the blind form was clasified as vulnerable (VU) by IUCN and (A) in NOM-059 SEMARNAT 2010 [102,103].

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Figure 1. The Pánuco Basin, in Eastern central Mexico, with four sub-basins (sensu INEGI, 2007). Map includes locations where records for the most diverse families, Cyprinidae, Cichlidae, and Poeciliidae, were obtained. “Others” refers to other families found in each location. Coordinates in universal transverse Mercator (UTM) units for zone 14 N.
Figure 1. The Pánuco Basin, in Eastern central Mexico, with four sub-basins (sensu INEGI, 2007). Map includes locations where records for the most diverse families, Cyprinidae, Cichlidae, and Poeciliidae, were obtained. “Others” refers to other families found in each location. Coordinates in universal transverse Mercator (UTM) units for zone 14 N.
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Figure 2. Multidimensional scaling (MDS) comparison (Jaccard values of similarity) of Pánuco River ichthyofauna between (a) time intervals and (b) sub-basins (see methods for details). Icons in black represent the centroids for each group with a similar shape.
Figure 2. Multidimensional scaling (MDS) comparison (Jaccard values of similarity) of Pánuco River ichthyofauna between (a) time intervals and (b) sub-basins (see methods for details). Icons in black represent the centroids for each group with a similar shape.
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Figure 3. Time interval and sub-basin dual clustering analysis results for the Pánuco River ichthyofauna. The numbers from 0 to 4 in the columns indicate the number of sub-basins where a species was recorded. Groups formed in analyses are indicated by a number to the left of each colored box. The tree to the right indicates similarity in distribution among species and species groups. The tree at the bottom of the image indicates similarity among time intervals.
Figure 3. Time interval and sub-basin dual clustering analysis results for the Pánuco River ichthyofauna. The numbers from 0 to 4 in the columns indicate the number of sub-basins where a species was recorded. Groups formed in analyses are indicated by a number to the left of each colored box. The tree to the right indicates similarity in distribution among species and species groups. The tree at the bottom of the image indicates similarity among time intervals.
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Table 1. Attributes of Pánuco River Basin fish species groups formed in cluster analyses. For each group, we present the number of species in the group; the number of natives, non-natives, and invasives; the number of species in each group categorized by IUCN or NOM 059 SEMARNAT 2010; and general characteristics for the group.
Table 1. Attributes of Pánuco River Basin fish species groups formed in cluster analyses. For each group, we present the number of species in the group; the number of natives, non-natives, and invasives; the number of species in each group categorized by IUCN or NOM 059 SEMARNAT 2010; and general characteristics for the group.
GroupSpecies in GroupNativeNon NativeInvasiveIUCN *NOM 059 SEMARNAT 2010 **Group Attributes
119172022Eight species were not found in later time intervals.
2761024Three species were not found in later time intervals.
3606520All species present through time intervals.
4862100All species present through time intervals.
519136078Species were lost between time intervals 4 and 5.
61183132All species present through time intervals.
710010432Nine species were introduced after time interval 3, but four were not found in the last time interval.
815411131Species were not reported after time interval 1.
* International Union for Conservation of Nature (IUCN). Species categories: NT = near threatened, VU = vulnerable, EN = endangered, CR = critically endangered. ** NORMA Oficial Mexicana NOM-059-SEMARNAT-2010. Species categories: Pr = subject to special protection, A = threatened, P = in danger of extinction.
Table 2. Fish species from the Pánuco Basin correlated with discriminant function analyses for time intervals (see text). Eigenvalues and % of variance explained in a function are shown. DF: Discriminant function.
Table 2. Fish species from the Pánuco Basin correlated with discriminant function analyses for time intervals (see text). Eigenvalues and % of variance explained in a function are shown. DF: Discriminant function.
SpeciesDF1DF2
Algansea tincella0.0385160.030990
Amatitlania nigrofasciata−0.006545−0.114626
Ataeniobius toweri0.0222370.017892
Carassius auratus−0.0076130.028727
Chirostoma grandocule0.0088910.310992
Coptodon rendalli0.0051330.179551
Coptodon zillii0.0088910.310992
Ctenopharyngodon idella0.035840−0.127134
Cyprinus carpio−0.029556−0.062774
Gambusia affinis0.0238310.103444
Gambusia marshi0.0243450.026311
Ictiobus bubalus0.0137310.063038
Notropis boucardi0.012446−0.089352
Eigenvalue126.947.05
% of variance92.795.1
Table 3. Fish species from the Pánuco Basin correlated with discriminant function analyses for sub-basins (see text). Eigenvalues and % of variance explained in each function are shown. DF: Discriminant function.
Table 3. Fish species from the Pánuco Basin correlated with discriminant function analyses for sub-basins (see text). Eigenvalues and % of variance explained in each function are shown. DF: Discriminant function.
SpeciesDF1DF2
Algansea tincella0.103136−0.044257
Amatitlania nigrofasciata0.0561620.165854
Ataeniobius toweri0.054143−0.333427
Carassius auratus0.0801270.099953
Chirostoma grandocule0.0010500.068697
Coptodon rendalli0.0229280.067710
Coptodon zillii0.0055920.038124
Ctenopharyngodon idella−0.001050−0.068697
Cyprinus carpio0.0620670.143948
Gambusia atrora0.0496870.212331
Gambusia marshi−0.0232920.029809
Gambusia panuco0.029366−0.127961
Ictiobus bubalus−0.010438−0.070169
Notropis boucardi0.013536−0.083357
Eigenvalue179.2919.86
% of variance87.679.7
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