Márcio J. Silva1,2,3 , Telton P. A. Ramos1,4, Fernando R. Carvalho5, Marcelo F. G. Brito6, Robson T. C. Ramos7, Ricardo S. Rosa8, Jorge I. Sánchez-Botero9, José L. C. Novaes10, Rodrigo S. Costa10 and Sergio M. Q. Lima1
Global aquatic ecosystems have been losing part of their biodiversity in response to increasingly deleterious anthropogenic pressure, caused mainly by rampant population growth, preposterous consumption of natural resources, energy production, and the absence of efficient management and conservation mechanisms (Abell et al., 2008; Barletta et al., 2010). This scenario is even more worrying in freshwater systems, which, besides having a smaller physical area, have been historically undergoing severe environmental alterations, such as damming, illegal water catchment, introduction of species and contamination by pesticides and effluents (L’vovich, White, 1990; Meybeck, 2003; Dudgeon, 2019). All these impacts have a cumulative effect by reducing habitat quality and quantity and increasing extinction risk for freshwater fishes, making those systems into one of the most threatened worldwide (Meybeck, 2003; Revenga et al., 2005; Abell et al., 2008; Reis et al., 2016; Castro, Polaz, 2020).
One of the main issues related to aquatic ecosystems is water scarcity, especially in arid and semiarid areas. When the demand for water increases and almost reaches the available limit, debates over management and attainment of new resources emerge as an attempt to converge on an integrated management model (L’vovich, White, 1990; Meybeck, 2003; Gupta, Van der Zaag, 2008). Some countries have solved this problem by expanding their hydrographic network through aqueducts and canals (Van der Zaag, 2007; Gupta, Van der Zaag, 2008). Currently, water transfers projects have started or are under discussion in South America, in the São Francisco Interbasin Water Transfer Project (SFR-IWT, in Brazil), Africa, in the Lesotho Highland Water Project (between Lesotho and South Africa) and Asia, in the South to North Water Diversion Project (SNWDP, in China), and in the Par Tapi Narmada Link Project (PTNLP, in India).These projects differ, mainly in the number of connected ecoregions, basins, canal length, and captured water volume (Brasil, 2004; India, 2017; Lesotho, 2020; Long et al., 2020).
However, such projects are considered as imminent threats to freshwater biodiversity (Albert et al., 2020) and face many criticisms and heated debates over the socio-economic benefits versus environmental issues they can cause (Meador, 1992; Muller, 1999; Dyrnes, Vatn, 2005; Pittock et al., 2009). The latter include species introductions, loss of local adaptations and biota homogenization, genetic introgression, competitive exclusion, hybridization, habitat modification (including terrestrial vegetation fragmentation by canals), and water availability and quality (Meador, 1992; Pittock et al., 2009; Albert et al., 2020).
Water shortage is one of the main problems in the Brazilian Northeast region, which is mostly inserted in the semiarid Caatinga (Lima et al., 2017). It is a highly impacted area, some of which is in the process of desertification (Albuquerque et al., 2012), and whose aquatic habitats are considered the most modified and threatened in the country (Silva et al., 2004). Recurrent droughts limit water supply and demand huge engineering projects (Rosa et al., 2004).
The idea to transpose waters from the rio São Francisco was introduced in 1847 by the engineer Marcos de Macedo to Emperor Dom Pedro II. In 1913, after the ‘Great Drought’ (1875-1879), the construction of a canal that would connect the São Francisco and Jaguaribe basins was outlined. Nevertheless, it became impracticable due to technical reasons, lack of financial resources and ignorance of its benefits (Andrade et al., 2011). After other frustrated attempts, in 2005 the project was redesigned and started to be known as the São Francisco Interbasin Water Transfer to the Northeastern Hydrographic Basins Project (SFR-IWT, Projeto de Integração do Rio São Francisco com as Bacias Hidrográficas do Nordeste Setentrional, in Portuguese) (Brasil, 2004).
The SFR-IWT aims to transfer 3.5% of the São Francisco basin water to the Jaguaribe, Apodi-Mossoró, Piranhas-Açu, and Paraíba do Norte basins, through a two-canal system (North and East Axis), aqueducts, tunnels, dams, and pumping stations, resulting in 720 km of extension (577 km, excepting the secondary canals, 357 km in the North Axis and 220 km in the East Axis), whose catchment areas are located in the lower-middle stretch of the São Francisco basin (Brasil, 2004). Since its approval in 2007 and the beginning of construction, in 2008 (Andrade et al., 2011), the project has faced many delays but is now almost concluded, with the East Axis in operation since March 2017 and the North Axis partially operating since February 2018 (Brasil, 2019). Besides the SFR-IWT, the São Francisco basin was artificially connected to the upper Paraná basin in the 1960s through the rio Piumhi, during the construction of the Furnas Hydroelectric Power Plant, which resulted in an input of fish fauna from the captured basin (Moreira-Filho, Buckup, 2005).
The SFR-IWT installation license was granted in 2007 based on an environmental impact study (Brasil, 2004). This report, written at the same time as publication of the seminal studies on Caatinga fish (Rosa et al., 2003, 2004; Rosa, 2004), came across taxonomic issues and species distribution inaccuracies, reflecting the incipient knowledge on this ichthyofauna. Recently, a global database of freshwater fish species listed by drainage channels included data from more than 3,000 basins; however, the Northeast of Brazil was indicated as spatial gap, with data available from few basins (Tedesco et al., 2017). This database is useful to evaluate non-native species’ influence on the native ichthyofauna, which are under homogenization processes (Tedesco et al., 2017). The limited information on the distributional ranges of the species also hampers evaluation of the conservation status of the species (Dias et al., 2016).
Due to climatic and edaphic conditions, which resulted in temporary rivers, the fish diversity of the Caatinga was underestimated until recently (Rosa et al., 2003). Lima et al. (2017) updated this list, increasing it to 386 species, 203 of them endemic to a single freshwater ecoregion (sensuAbell et al., 2008), and 33 threatened species. However, the biological diversity and the conservation status of its biota are still poorly known, and inventories should be performed on a regional scale to support public conservation policies (Rosa et al., 2004; Lévêque et al., 2005, 2008; Tedesco et al., 2017). The Caatinga’s hydrography is composed of four freshwater ecoregions: Maranhão-Piauí (MAPE), Mid-Northeastern Caatinga (MNCE), São Francisco (SFRE), and Northeastern Atlantic Forest (NAFE) (Rosa et al., 2003; Albert et al., 2011; Lima et al., 2017). Most MNCE basins exhibit an intermittent regime and small to medium extensions (Rosa et al., 2004). They also have lower fish species richness and endemism (88 and 38, respectively) when compared to the adjacent SFRE (211 and 135) and to the MAPE (151 and 54) (Albert et al., 2011; Ramos et al., 2014; Silva et al., 2015; Reis et al., 2016). The high endemism level of these ecoregions suggests ancient separation and low connectivity among the basins (Albert, Carvalho, 2011), but these numbers are still partial, especially for the MNCE, since the regional collections are scarcely digitalized, and only a few species of this ecoregion, are available (Buckup et al., 2007; Lévêque et al., 2008; Langeani et al., 2009).
Regarding the SFR-IWT basins, there is a huge data deficiency, and comparative studies are paramount to inform which species are endemic, naturally shared and potentially invasive before the artificial connection (Langeani et al., 2009). This urgency encouraged the present comprehensive study of the SFR-IWT’s freshwater fish fauna. Therefore, the purpose of this study was to elaborate an original ichthyofaunal species list of the basins encompassed in the SFR-IWT, proposing a taxonomic nomenclatural standardization, and indicating which species are endemic, endangered, non-native, and naturally shared between basins and ecoregions. Notwithstanding, this baseline is not definitive and should be refined and updated regularly. Besides that, it may help in the detection of possible changes in fish composition resulting from the SFR-IWT and the proposition of public policies for the conservation of Caatinga ichthyofauna.
Material and methods
Information source. The freshwater fish species occurrence data comprised the rio São Francisco lower-middle stretch, the SFR-IWT catchment area in SFRE; and receptor’s drainages of the Jaguaribe (JAG), Apodi-Mossoró (APO), Piranhas-Açu (PIA), and Paraíba do Norte (PAR) river basins in the MNCE. The map was produced with QuantumGIS free program (www.qgis.org). Calculations of the drainage area and number of municipalities were done using georeferenced shapefiles of the National Water Agency (Brasil, 2014a) and Ministry of the Environment (Brasil, 2014b), while the São Francisco Hydrographic Basin Committee provided the SFR-IWT canal trails (CBHSF, 2014) (Fig. 1).
FIGURE 1 | Sampling sites of the freshwater fish species in the São Francisco Interbasin Water Transfer Project basins in the Brazilian semiarid.
The São Francisco basin and ecoregion has an approximate area of 640,000 km². Its main river, the São Francisco, is the largest in the Northeast region, and the third in Brazil (Rosa et al., 2003). It is subdivided in to four stretches: upper, middle, lower-middle, and lower (Brasil, 2014a). Herein, only records in the lower-middle stretch (112,093.68 km², 17.51% of São Francisco basin and 42.52% of SFR-IWT) were considered, and this stretch is under direct influence of the SFR-IWT, including 98 municipalities, from downstream Sobradinho Dam reservoir (Sobradinho Municipality, Bahia State) to the upstream Lajeadinho Stream (Canindé de São Francisco Municipality, Sergipe State), or approximately 50 km downstream of Paulo Afonso Dam (Brasil, 2014a) (Fig. 1). In this semiarid area, most tributaries of the São Francisco are intermittent (Rosa et al., 2003), and some of them (Moxotó, Pajeú, Terra Nova, and Brígida rivers) will also receive water inflow from the main São Francisco channel (Lima, 2005).
The receptor basins are the four main drainage areas of the Mid-Northeatern Caatinga ecoregion (MNCE), presented in the west-east direction. The Jaguaribe basin supplies water to 88 municipalities of Ceará State and is the largest MNCE basin, with an area of 74,077.01 km² (28.10% of SFR-IWT). Besides the Jaguaribe River (633 km of extension), the basin includes tributaries, such as the Banabuiú and Salgado rivers (Brasil, 2014a). The Apodi-Mossoró basin encompasses 68 municipalities in Rio Grande do Norte State with an area of 14,303.71 km² (5.43% of SFR-IWT), and approximately 200 km of extension (Brasil, 2014a). Extending about 350 km, the Piranhas-Açu basin represents the second largest MNCE basin (43,141.54 km², 16.37% of SFR-IWT), draining 158 municipalities in Paraíba and Rio Grande do Norte states (Brasil, 2014a). These three basins will receive water from the SFR-IWT North Axis (Brasil, 2004) (Fig. 1). Lastly, the Paraíba do Norte basin, with 19,977.48 km² (7.58% of SFR-IWT) and 280 km length in 90 municipalities (Brasil, 2014a) in Paraíba State, is the largest one in the MNCE that flows to the east coast (the other ones drain to the north) (Brasil, 2019) (Fig. 1).
Species records. Species occurrences were obtained through latitude and longitude data, taking into account strictly freshwater fish families (Buckup et al., 2007). In the few cases in which the geographical coordinates were not available in the original source, they were approximated using the GeoNames website (www.geonames.org). All records were made before any water input from the SFR-IWT canals in March 2017.
Primary data were obtained from collected and deposited material in ichthyological collections at the Federal Universities of Paraíba (UFPB, 129 localities – 56.09%) and Rio Grande do Norte (UFRN, 101 – 43.91%). All locality data were listed in the supplementary material (S1). Distinct active (trawls, dip nets, sieves, fishhooks, and cast nets) and passive (gill nets and traps) fishing methods were used to reduce selectivity (Uieda, Castro, 1999).
Secondary data (76 localities) were acquired in two steps: 1) data from digitalized ichthyological collections available in speciesLink, PRONEX/NEODAT, and Portal da Biodiversidade (www.splink.org.br, www.mnrj.ufrj.br/pronex/, and https://portaldabiodiversidade.icmbio.gov.br/portal/), and 2) literature review (e.g.Reis et al., 2003; Buckup et al., 2007). At this stage, the bibliographic databases Web of Science and Google Scholar were consulted during searches of species records in the SFR-IWT basins (filtering dubious occurrences) after January 2006, the time frame used by Buckup et al. (2007), until March 2017, current frame (e.g.Luz et al., 2012; Nascimento et al., 2014), including new species descriptions (e.g.Ribeiro, Lucena, 2006; Lucena, 2007; Lima, Britski, 2007; Ramos et al., 2013; Zawadzki et al., 2017). The abbreviation “aff.” was used for species that have affinity with, but should be distinct from, the nominal taxon to which they are currently assigned.
Taxonomic validation. Nominal species validity, synonyms, and systematic classification were carried out according to Fricke et al. (2020). Some species with uncertain taxonomic status were considered as species inquirendae, following the recommendation of Lima et al. (2017). Specific studies on species introduction in the Northeast region were examined in order to determine non-native species (Gurgel, Fernando, 1994; DNOCS, 2002; Rosa et al., 2003; Mattheus, 2005; Leão et al., 2011; Paiva, Mesquita, 2013). The Brazilian list of endangered fish and aquatic invertebrates was consulted to indicate the threatened ones (Brasil, 2014c), given that it follows IUCN parameters. Reis et al. (2003), Buckup et al. (2007), Fricke et al. (2020) and Lima et al. (2017) were examined in order to determine the endemic species, defined herein as those restricted to a single basin or hydrographic ecoregion.
All specimens were deposited in one of these museums: ANSP (The Academy of Natural Sciences, Drexel University); FMNH (Field Museum of Natural History); LIRP (Laboratório de Ictiologia de Ribeirão Preto); MCP (Museu de Ciências e Tecnologia da Pontifícia Universidade Católica do Rio Grande do Sul); MNHN (Muséum National d’Histoire Naturelle); MNRJ (Museu Nacional, Universidade Federal do Rio de Janeiro); MZUEL (Museu de Zoologia, Universidade Estadual de Londrina); MZUSP (Museu de Zoologia, Universidade de São Paulo); NMW (Naturhistorisches Museum, Wien); NUPELIA (Núcleo de Pesquisa em Limnologia, Ictiologia e Aquicultura); UFPB (Universidade Federal da Paraíba); UFRN (Universidade Federal do Rio Grande do Norte); UMMZ (University of Michigan Museum of Zoology); ZMB (Museum für Naturkunde). All lots are listed in the supplementary material (S2).
Spatial patterns of species richness. All species inquirendae, and those of the secondary and vicarious divisions families (e.g. Sciaenidae, Gobiidae, Clupeidae, Engraulidae) (sensuMyers, 1937) were removed from comparisons to avoid inflating the number of shared species due to taxonomic uncertainty or possible marine dispersion. However, the distribution of these species in literature was presented in S3 (available only in the online version) for future research. For the evaluation of spatial patterns of richness, each hydrographic basin had its species-area relationship calculated for native and endemic species (Albert et al., 2011). This relationship is extensively used as a way of comparing distinct and size-diverse ecosystems worldwide (Arrhenius, 1921; Connor, McCoy, 1979). Thus, in each region, the number of species is correlated with their spatial extent, through a function of type S=S0Ab. Where S is the number of species in area A, S0 is proportional species density (i.e., species richness per unit area), and b is the species-area scaling exponent, often with values in the range 0.25-0.50 (Dengler, 2009). Since the scaling exponent b deﬁnes the slope of the species-area regression, it may be interpreted as a measure of gamma diversity among areas, with higher values indicating greater differences in the taxonomic composition of areas. The similarities of native species composition between river basins were calculated using Jaccard’s similarity coefficient index, using the following formula J=(c/(a+b+c)).100, where c is the number of fish species existing at both sampling sites and a and b are the number of fish species at different sampling sites. This index takes into account only the values of presence and absence of species in each basin (Lévêque et al., 2013).
Species richness and species-area relationships. In total, 17,002 lots of fish were compiled, of which 3,331 (2,729 primary data) were selected and recorded in 306 sampling sites (230 primaries), 117 (66 primaries) in SFRE (lower-middle São Francisco basin) and 189 (164 primaries) in the MNCE. In the receptor drainages (MNCE’s localities), there were 56 (50 primaries) in the Jaguaribe (JAG), 30 (22) in the Apodi-Mossoró (APO), 59 (all primaries) in the Piranhas-Açu (PIA), and 44 (all primaries) in the Paraíba do Norte basins (PAR) (Figs. 1-2).
FIGURE 2 | Sampling sites in the São Francisco Interbasin Water Transfer Project basins in the Brazilian semiarid. A = Canals under construction near the rio São Francisco main channel, and B = near Sertânia, Pernambuco State (PE), C = Rio Pajeú, tributary of the São Francisco basin, PE, D = Rio São Francisco near Petrolina, PE, E = Temporary pool in rio Jaguaribe basin in Russas, Ceará State (CE), F = Rio Jaguaribe in Crato, CE, G = Rio Apodi-Mossoró in Pau dos Ferros, Rio Grande do Norte State (RN), H = Rio Apodi-Mossoró in Pau dos Ferros, RN, I = Rio Seridó, tributary of the Piranhas-Açu basin in Caicó, RN, J = Rio Piranhas-Açu, Jardim de Piranhas, RN, K = Rio Paraíba do Norte in Barra de Santana, Paraíba State (PB), L = Rio Paraíba do Norte in São João do Cariri, PB.
In this study, 121 valid freshwater fish species were recorded, from 25 families and seven orders, or 111, 23 and six, respectively, considering only the native species (Tab. 1, Fig. 3A-I). Additionally, five species belonging to families of the vicarious divisions were found, but disregarded in the list and analyses: three native, Anchoviella vaillanti (Steindachner, 1908) endemic to SFRE, A. lepidentostole (Fowler, 1911) present in JAG, and Awaous tajasica (Lichtenstein, 1822) recorded in PAR, and two introduced ones, Plagioscion auratus (Castelnau, 1855) in SFRE and P. squamosissimus (Heckel, 1840), recorded in all basins of the SFR-IWT, except in PAR (Alves et al., 2011; Leão et al., 2011). Furthermore, six species inquirendae were listed, Psalidodon rivularis (Lütken, 1875), Pseudancistrus papariae Fowler, 1941, Pimelodella papariae (Fowler, 1941), P. witmeri Fowler, 1941, Hypostomus carvalhoi (Miranda Ribeiro, 1937), and H. jaguribensis (Fowler, 1915) (S3).
Five endangered species were recorded, three of them in SFRE, Lophiosilurus alexandri Steindachner, 1876 as vulnerable, Conorhynchos conirostris (Valenciennes, 1840) as endangered (EN), and Hypsolebias flavicaudatus (Costa & Brasil, 1990) as critically endangered), and two in MNCE, Apareiodon davisi Fowler, 1941 (EN) and Parotocinclus spilurus (Fowler, 1941) (EN) (Tab. 1 , Fig. 3F). Eleven non-native species were recorded, eight of which occur in SFRE and MNCE receptor basins (Colossoma macropomum, Parachromis managuensis, Poecilia reticulata, Astronotus ocellatus, Cichla monoculus, C. kelberi, Oreochromis niloticus, and Coptodon rendalli); the last six exist in all SFR-IWT basins, and three only in the MNCE (Arapaima gigas, Megaleporinus obtusidens, native in SFRE, and Xiphophorus helleri) (Tab. 1, Fig. 3J-L).
TABLE 1 | List of freshwater fish species recorded in the São Francisco Interbasin Water Transfer Project basins in the Brazilian semiarid. SFRE = São Francisco Ecoregion (lower-middle São Francisco basin); MNCE = Mid-Northeastern Caatinga Ecoregion; JAG = Jaguaribe basin; APO = Apodi-Mossoró basin; PIA = Piranhas-Açu basin; PAR = Paraíba do Norte basin; P = Primary data; S = Secondary data; NNA = Non-Native Species; EN = Endangered; VU = Vulnerable; CR = Critically Endangered. Fish classification follows Fricke et al. (2020).
FIGURE 3 | Freshwater fish species from the São Francisco Interbasin Water Transfer Project basins in the Brazilian semiarid. A = Hemigrammus brevis, endemic species of São Francisco Ecoregion (SFRE); B = Moenkhausia costae and C = Psellogrammus kennedyi, shared species between SFRE and Mid-Northeastern Caatinga Ecoregion (MNCE); D = Aspidoras menezesi, endemic species of Jaguaribe basin (JAG) ; E = Hypostomus sertanejo, endemic species of MNCE; F = Parotocinclus spilurus, endemic and endangered species of JAG; G = Tatia bockmanni, endemic species of SFRE; H = Cichlasoma orientale, shared species from all basins of SFR-IWT; I = Geophagus brasiliensis, shared species between SFRE and MNCE; J = Colossoma macropomum, non-native species shared between SFRE and Piranhas-Açu basin; K = Parachromis managuensis, non-native species shared between SFRE and Paraíba do Norte basin; L = Xiphophorus helleri, non-native species of JAG.
Regarding the hydrographic basins, considering only native species, the highest richness (78, corresponding to 70.27%) was recorded in the SFRE donor basin, while the MNCE’s receptor basins accounted for 61 species (54.95%). Of those, 50 species (44.05% of total and 81.97% of MNCE) were recorded in JAG, 39 (35.14% and 63.93%) in PIA, 36 (32.43% and 59.02%) in PAR, and 32 (28.83% and 52.46%) in APO (Tab. 2). The species-area relationship calculation indicated that the SFRE (lower-middle stretch) exhibits the highest native species density (1.75), followed by PAR (1.42), APO (1.41), JAG (1.29), MNCE (1.24, all receptor basins) and PIA (1.20) (Tab. 3). Considering only the endemic species, the following values were obtained: SFRE (0.52), MNCE (0.26), JAG (0.05), PAR (0.04), and PIA (0.03). The APO basin did not contain any endemic species, and its higher species-area value might be related to its smaller size in comparison to the other basins (Tab. 3).
TABLE 2 | Number and percentage of shared native fish species in the São Francisco Interbasin Water Transfer Project basins in the Brazilian semiarid. Number of species in each basin and ecoregion on the diagonal in bold. SFRE = São Francisco Ecoregion (lower-middle São Francisco basin); MNCE = Mid-Northeastern Caatinga Ecoregion (JAG+APO+PIA+PAR); JAG = Jaguaribe basin; APO = Apodi-Mossoró basin; PIA = Piranhas-Açu basin; PAR = Paraíba do Norte basin.