Changes in fish species composition in the middle and lower Tietê River ( São Paulo , Brazil ) throughout the centuries , emphasizing rheophilic and introduced species

Aim: This paper is aimed at describing the changes of fish species in the middle and lower courses of the Tietê River, emphasizing rheophilic and invasive fish species as well as identifying the causes for such alterations. Methods: Data collection consisted in: intense revision of publications, dissertations and thesis regarding the subject; information at the Zoology Museum at USP (MZUSP); revision in species identification through MUZUSP collection; historical survey of introduced species based on the literature and samplings in the years of 2000 and 2001. Results: The main impacts identified in the Tietê River with consequence to the ichthyofauna were: domestic and industrial pollution, deforestation, damming, course rectification, silting and species introduction. From the 80 species identified in the study area, 28 were invasive. Many fish species have been introduced in the Tietê River since the late 19th Century with carpa (Cyprinus carpio) being the first one, followed by the introduction of black bass (Mycropterus salmonoides) at the beginning of 20th Century. Other species such as corvina (Plagioscion squamosissimus) have been introduced by electricity companies, which has contributed to the species composition changes. Migratory species as dourado (Salminus brasiliensis), pacú (Piaractus mesopotamicus) and pintado (Pseudoplatystoma corruscans), which used to be abundant have become rare or absent after the construction of reservoirs, mainly because reservoirs in cascade have been built. Piracanjuba (Brycon orbignyanus), typically herbivore species, had its stock decreased due to the lack of ciliary vegetation and damming. Conclusions: Following the building of the reservoirs there have been important alterations in the composition of ichthyofauna, leading to the nearly complete absence of migratory species and the prevalent species are the ones which adapted to the new conditions. In addition to the damming, lack of ciliary vegetation and pollution also caused alterations in the ichthyological community.

and the operational procedures of the reservoir (Agostinho et al., 1995).
Furthermore, the impact over the fish community will depend on several factors, such as the type and size of the river, of great importance, the location and maintenance of vegetal coverage in the margins, the presence of tributaries used for the rheophilic reproduction and the effect of the reservoirs in cascade.Many rheophilic species may survive in the reservoir using the tributaries for reproduction (Smith et al., 2014).
Besides the impacts caused by the construction of reservoirs and their operation, the fish community is subject to several impacts which contribute heavily to the loss of species, as well as the decrease of riparian vegetation, pollution and the introduction of species, which may lead to the reduction of its biomass and abundance and consequently its complete extinction (Smith et al., 2002;Vitule et al., 2009).
There are some studies regarding the composition of the ichthyofauna concerning the Middle and Lower Tietê River.Some examples, Monteiro (1953) evaluated the contribution to the fishery study in the Piracibaba River, and Rocha et al. (2011) described animal invaders in São Paulo state reservoirs.The impacts of the reservoirs and its gradients of middle and lower Tietê, fishing modification due to dam, pollution and the introduction of fish species (Smith et al., 2002(Smith et al., , 2003a(Smith et al., , 2014;;Moretto et al., 2008), and large reservoirs as ecological barriers

Introduction
The reservoirs consist in important artificial ecosystems that alter the hydrological and ecological characteristics of a river (Tundisi, 1993), being regulated by the following factors: morphometry, seasoning, operation system, flow rate and residence time.Such factors not only alter the physical and chemical characteristics of the water (Straškraba & Tundisi, 2000;Smith et al., 2014) but also shape the structure of the fish communities (Pelicice et al., 2015).The reservoirs are the dominant environment in the Paraná River Basin and the fish shoals inhabiting these places have been altered from the original ones (Agostinho et al., 1995).
The creation of a new ecosystem, which becomes lentic, somehow constitutes another impact over the remaining communities in the upstream of the damming.This community will suffer modifications such as the reduction of some rheofilic species, which will be replaced by lentic adaptable species, for instance, the Curimatidae (Castro & Arcifa, 1987;Smith & Petrere Júnior, 2001;Agostinho et al., 2008).
Considering all the impact here presented, this paper describes the alterations in the composition of fish species along years, through a historical survey of species introduction and several changes as well as presenting the impacts suffered by the Tietê River in addition to the existing dams.

Material and Methods
The area chosen for the study is in the middle and lower courses of the Tietê River (Figure 1).This river is one of the most important water bodies of São Paulo State, crossing from the Serra do Mar mountain chain to the Paraná River.Its total length is 1,150 Km and the great unevenness of its course was used for the construction of dams to produce electricity.Currently it is a navigable river from the Jupiá Dam in the Paraná River (40Km), and the stretches between the dams of Barra Bonita and Nova Avanhandava (443 Km) (Smith et al., 2003a).
The data presented in this paper were obtained through revision of publications, dissertations and thesis accomplished between 1953 and 2015, in the study area as well as a survey conducted at the Zoology Museum at USP, Section of Fishes, aiming at evaluating all the species which have already been collected in the study area and possibly deposited.The referred literature was chosen according to the presence of the following key words: Tietê river, damming, fish ecology, fish diversity, dam impacts, fish management, fish conservation, fish introduction, fish community, native species, cascading reservoirs, fishway, fish migration.Was used the databases ISI Web of Knowledge, Google Scholar and Scopus.
Moreover, a revision of the species identification was made in the literature found.Such revision was based on papers done in the study area, intending to rectify or update the species identification made by other authors and having a more reliable and complete list of species occurring in the study area.Another important point raised was related to the introduced species, whose survey made it possible to identify the invasive species with greater accuracy, their original occurrence and how they have been introduced.
In order to complete the data we performed samplings in January 2000 (rainy season), January 2001 (rainy season) and in July 2001 (dry season).The samplings were made along the middle and lower courses of the Tietê River with two sets of fishing nets containing 8 nets with different mesh sizes (3, 4, 5, 6, 7, 8, 10 and 12 cm, between opposed knots), dip net and dragging nets.The sets were put in the reservoir and tributaries edge area in different depths (surface half-water and half water-deep).Besides, dip nets were used to collect fish with macrophyte and vegetation also located in the edge area and dragging net in river beaches or places allowing their passage.The fishes which were captured were fixed in formaline 10% and conserved in alcohol 70%, being stored in plastic recipients and transported to the Núcleo de Estudos de Ecossistemas Aquaticos (NEEA), of the the Centro de Recursos Hídricos e Estudos Ambientais (CRHEA), of the Departamento de Hidráulica e Saneamento (SHS), in the Escola de Engenharia de São Carlos (EESC), Universidade de São Paulo (USP) in São Carlos, São Paulo State, where they were identified using identification keys (Britski, 1972;Britski et al., 1984;Garutti & Britski, 2000).Afterwards, species were confirmed in comparison to the material deposited at the Museum of Zoology at USP, Fish Section.

Results
The modifications in the Tietê River and its ichthyofauna of throughout the years occurred due to domestic and industrial pollution, deforestation, damming, course rectification, silting and species introduction (Table 1 and Table 2).In the 17th Century, the ciliary forest had already been damaged in the upper course of the Tietê River and more recently the dammings in the middle and lower courses of the Tietê River have strengthened the modification in the composition of fish species.Such impacts caused a series of modifications in the fish population and communities, leading to severe alterations in the composition of species along the Tietê River, as dominance of exotic species and the presence of species that did not occurs previously.
By using data presented in Machado et al. (1968), CNEC (1969) and Nóbrega (1978), it was possible to verify that in the 17th, 18th and 19th Centuries migratory species were common, in addition to the more commonly found species today (Table 3).From the 19th Century on, migratory species became less abundant in the stretch crossing São Paulo City, causing a simplification of the ichthyofauna.
In the first half of the 20th Century, it was still possible to find migrator y species as dourado (Salminus brasiliensis), pacú (Piaractus mesopotamicus), pintado (Pseudoplatystoma corruscans) and piracanjuba (Brycon orbynianus) in the stretches of the middle and lower course of the Tietê River, before the constructions of the reservoirs.From the sixties on, because of dams in cascade, such species began to occur in reduced number resulting in the almost complete absence from the eighties on.Nonetheless, curimbatá (Prochilodus lineatus) and tabarana (Salminus hilarii) may still be found in the Tietê River.
Information regarding before the building of the dams is scarce and it may be found in a few papers such as Monteiro's from 1953 about the Piracicaba River but it mentions the Tietê River as far as Barra Bonita reservoir.There are also other studies which date back to the sixties, when the abundance of migratory species such as dourado (Salminus brasiliensis), pintado (Pseudoplatystoma corruscans), jaú (Zungaro jahu) e piracanjuba (Brycon orbygnianus) was reported in fishing.Such species became rare after the dammings and recurrent impacts being suffered by the Tietê River.In the Tietê River, from the 80 species which were identified 28 have been introduced (Table 4).

Discussion
The main modifications over time in the middle and lower courses of the Tietê River were the reduction of migratory species and the introduction of species.Although there was a change in the fish community, the number of species remained stable throughout the studied period.The dams in the Tietê River prevent the migration of some species, such as jaú (Zungaro jahu), pintado (Pseudoplatystoma corruscans) and dourado (Salminus maxillosus), among others.These species cannot go upstream and migrate to areas where they can reproduce.Smith et al. (2002), shows a reduction of migratory species caught professionally in the area where Barra Bonita Reservoir is situated.According to Monteiro, in 1953, prior to the dam constructions, a great amount of curimbatá (Prochilodus lineatus), dourado (Salminus brasiliensis), jaú (Zungaro jahu) and pintado (Pseudoplatystoma corruscans) was caught.In 1989, after the building of the dams, such amount dropped drastically and many of these species disappeared from this river.Agostinho et al. (1999) also noted alterations in the fish catching from 1977 to 1997 in the Paraná River, showing that before the dam constructions, most species present there were migratory, such as Zungaro jahu, Salminus brasiliensis and Prochilodus lineatus and after the damming non-migratory and invasive species as Pterodoras granulosus (Valenciennes, 1821), Plagioscion squamosissimus and Hypophthalmus edentatus were prevailing.
The change in fish community seems to be the main characteristic of damming regions.
Table 2. Main impacts in the middle and lower courses of the Tietê River and their consequences to the ichthyofauna.

Impacts
Consequence to the fishes Consequence to the populations and communities Domestic Pollution Alteration in the enzymatic activities (causing stress), in activities (swimming), feeding, mucus production and death.
Increase in eggs, young and adult fish death, reduction of abundance, richness and diversity; interference in the distribution of abundance and decrease in the community's complexity.Industrial Pollution Alteration in the enzymatic activities (causing stress), in the activities (swimming) feeding, mucus production and death.
Increase in eggs, fingerlings and adult fish death, reduction of abundance, richness and diversity; interference in the distribution of abundance and decrease in the community complexity.Deforestation Decrease in feeding resources, shelters and reproduction.
Reduction of abundance, richness and diversity, interference in the distribution of abundance, and decrease in the complexity of the community.

Siltings
Decrease in feeding resources, shelters and reproduction.
Damage in eggs and fingerlings' development.

Dammings
Interference in the migratory species reproduction.
Increase of predation, reduction of abundance, richness and diversity of species, interference in the distribution of abundance and decrease in the community's complexity.Course Rectification Decrease in feeding resources, shelters and reproduction.
Increase in the eggs and juveniles' death.

Silt removal
Decrease in feeding resources, shelters and reproduction.
Increase in the eggs and juveniles' death.

Introduction of species
Transmission of diseases and parasites, competition and predation.
Reduction of abundance, richness and diversity, interference in the distribution of abundance, and decrease in the complexity of the community.
Acta Limnologica Brasiliensia, 2018, vol. 30, e310 As also observed in the Paraná River by Agostinho et al. (1999), migratory species were abundant in the Tietê River before the damming.Currently non-migratory and introduced species are prevalent.Besides, fishermen emphasize that fish such as dourado and pintado are rarely captured and composition of species in fishing has changed greatly over the last years due to the damming and the introduction of exotic and alien species, increasing the capture of introduced species, wild species and small-sized species instead of large-sized species which have higher price (Smith, 2006).The loss of riparian vegetation contributed to the alteration of the species composition, decreasing the piracanjuba population (Brycon orbygnianus), since those are typically herbivore.Such loss also resulted in the almost complete disappearance of other species, such as pacú (Piaractus mesopotamicus) and pacuzinho (Myleus tiete).Along with those impacts it is important to highlight the introduction of species in the Tietê River.Based on information from Monteiro (1953) and Smith et al. (2002Smith et al. ( , 2003a)).Changes in fish species composition...
Acta Limnologica Brasiliensia, 2018, vol.30, e310   Agostinho et al. (1992) claimed that in reservoirs there is a change in the composition and structure of fish assembly, featuring excessive increase of some species and decrease or even extinction of others.The clearest response from the fish community in dams was not the disappearance of species but the modification in their structure.Such result is like the one obtained for the Tietê River where several migratory species disappeared.Besides the damming, the loss of species is the result of high deforestation and pollution rates (Smith et al., 2003a).In the Três Irmãos Reservoir it is difficult to catch lambaris, Astyanax lacustris Lütken, 1875, Astyanax fasciatus (Cuvier 1819) and cará (Geophagus brasiliensis), forage species which have nearly disappeared as a consequence of the construction of the reservoir and the pressure caused by the introduced species and the increase of population of other species such as pirambeba (Serrasalmus maculatus).
Some species are benefited by damming, as the small-sized ones with fractional spawning, non-migratory and able to use more abundant resources in the reservoirs, such as debris, higher plants, algae and fish.Examples of such species are saguirus (Cyphocharax modestus and Steindachnerina insculpta) and lambaris (Astyanax lacustris, Astyanax fasciatus) and Moenkhausia intermedia) which may be found in the upper course of the Paraná River Basin.These species complete their reproductive cycle in the reservoirs themselves or in their influence area.For these species, there was a increase of the abundance due to the modification in the ecosystem which was lotic and became lentic, making the conditions more favorable (Castro & Arcifa, 1987).
The construction of reservoirs boosted especially the introduction of invasive species from 1960 on.Energy companies were responsible for introducing such species, aiming at improving fishing activity since several native species such as dourado (Salminus maxillosus), pintado (Pseudoplatystoma corruscans), jaú (Zungaro jahu) and piracanjuba (Brycon orbygnianus), had had their stocks reduced (Smith et al., 2002(Smith et al., , 2003a)).It is important to point out that the deforestation of ciliary forest and pollution has also contributed to this reality.
Another aspect to be discussed is that damming eliminates natural obstacles that prevented some fish species to move on to drainage (Pelicice et al., 2015).In Brazil, a typical case refers to the Sete Quedas Falls in the Paraná River.Those waterfalls were flooded by the Itaipu Reservoir and were no longer an obstacle to the aquatic fauna found in the lower course of the Paraná River.Thus, some species with restrict distribution began to occupy upstream areas following the building of the reservoirs.
In the past, the introduction of species was regarded as an interesting activity to increase commercial fishing.Today though, it is highly agreed that such practice is not advisable, and it may have contributed to the reduction and even disappearance of native species (Hilsdorf & Petrere, 2002).The impacts brought about by exotic and alien species are little known in aquatic Brazilian ecosystems.Despite, information about possible signs of impact may already be found.The tucunaré, species from the Amazon, is considered a natural enemy to native species (Rocha et al., 2011) because it caused several species to end in a lake (Zaret & Paine, 1973).Furthermore, tucunaré is "good for fishermen", but extremely damaging to the environment.
There are many negative examples imposed by the introduction of fish species.Amongst them are the loss of species, the reduction of the amount of fish caught and alteration in the environment due to the decrease of spawning areas and even eutrophication (Welcomme, 1988;Fernando, 1991;Ross, 1991;Agostinho & Julio Júnior, 1996;Smith et al., 2003a).Such effect occurs especially when piscivore species are introduced pressuring native species either for predation or for competition.Besides, the introduced species may behave differently from what had been expected, occupying niches that are distinct from their regular ones.
Therefore, the damming in middle and lower courses of the Tietê River caused an important change in fish species composition, since many migratory species are no longer found in these stretches and the species which take advantage from the lentic environment are predominant.Besides all impacts caused by the damming and introduction of exotic species, the middle and lower courses of the Tietê River also suffer with different sources of pollution specially came from the São Paulo city, silting and lack of riparian vegetation.All of those factors contribute to changes in the composition of ichthyofauna throughout the years.

Figure 1 .
Figure 1.Location of the reservoirs, main tributaries and distribution of the sampling stations in the Tietê River, SP.
Limnologica Brasiliensia, 2018, vol.30, e310 tilápias were introduced in São Paulo State in 1952 by São Paulo Light, aiming at populating the dam on the upper part of the Serra do Mar mountain chain.The corvina (Plagioscion squamosissimus) was introduced in São Paulo state in 1966 by CESP, in the Pardo River, reaching the Grande River and Paraná River and in Ilha Solteira and Jupiá reservoirs, occupying Tietê River

Table 1 .
Main impacts in the middle and lower courses of the Tietê River and their consequences to the river.

Table 3 .
Main fish species captured by fishing (amateur, sports and experimental) in the Tietê River, SP, Brazil, from the 17th Century to the current days.

Table 4 .
Species of fish introduced in the middle and lower courses of the Tietê River, SP, Brazil.