Abiotic variables in the Guapi-Macacu River
In the Guapi-Macacu River, salinity was higher downstream in both seasons, while the values of DO and pH were higher in the dry season upstream. Partially similar results were reported by Macêdo et al. (2000) in the Rio Formoso estuary (Pernambuco, Brazil), which detected the highest pH values in the lower estuarine area, beyond has higher DO and salinity. According to Macêdo et al. (2000), salinity and oxygenation levels are influenced by tidal cycles and photosynthesis and respiration rates. The existing neutralization capacity in the aquatic ecosystem due to the buffer effect prevents wide pH variations. Therefore, maximum values did obtain in areas with more significant saline influence. In the Guapi-Macacu River, the highest salinity at the mouth of the Guanabara Bay is expected because it is a coastal segment, and its intensity may vary with the rainy season, which favors its dilution. The higher DO and pH rates reflect a season without rain, with greater water transparency, favoring photosynthesis that removes CO2 raising the pH of the water due to the consumption of H+ ions.
When analyzed individually, it observed that temperature and pH were the environmental attributes that were not related to the different segments of the river but seasons. The highest temperature in the rainy season corresponds to the hottest season of the year in South America. However, there is collinearity of environmental attributes. When they are presented in the reduced model and correlated with species abundances, pH reveals as a variable with high significance for the downstream area, probably due to its higher value in the dry season. The association of the other variables analyzed, such as the predominance of increased transparency in the intermediate region of the river, contributed to a better distinction between the river segments in the dry and rainy seasons, corroborating the environmental characteristics of the Guapi-Macacu River in the Guapimirim EPA, and serving as predictors for related fish species in this habitat. According to Blaber (2000), fish from tropical estuaries are subject to a range of interactions of physicochemical and biological factors that determine their patterns of occurrence, distribution, and movement. According to this author, in the Rio Formoso estuary (Pernambuco, Brazil), the temperature, salinity, pH, and dissolved oxygen were higher in the lower estuarine zone and dry season. In estuarine regions of Pernambuco, seasonal variations in water temperature and salinity are well evidenced, with the highest values being recorded in the dry season (Macêdo et al., 2004).
However, deficient levels of DO can be seen in the area downstream of the river, especially in the rainy season, coinciding with the lowest richness and abundance recorded. For Edokpayi et al. (2017), levels of DO concentrations below 5.0 mg/L adversely affect aquatic life. Furthermore, during the rainy season, Guanabara Bay drags organic materials and concentrates contamination during the dry season to the area downstream of the Guapi-Macacu River. In addition to the resuspension of sediments, explain less oxygenation during the wet season in this area.
The fish assemblage of the Guapi-Macacu River
The fish assemblage of the Guapi-Macacu River, within the Guapimirim EPA and its Buffer Zone, has freshwater species with marine species, many of which are euryhaline. Marine species were concentrated in the lower part of the river (downstream), at the mouth of the Guanabara Bay, with some species migrating to inland areas, such as bass, mullet, carapebas, and croakers. This segment was constituted by resident species, marine and freshwater migrants, which use the estuaries as feeding areas, for rearing larvae and juveniles, or for reproduction (Blaber, 2000). These habitats favor the presence of various fish populations on their margins (Vidy, 2000), consisting mainly of juveniles of marine species (Rozas & Zimmerman, 2000). The greater abundance of fish downstream of the Guapi-Macacu River is probably due to the food availability from primary production, structural complexity of mangrove vegetation, which provides refuge, especially for young fish, and high water turbidity. According to Loebman & Vieira (2005), the structure of the tropical estuarine fish fauna varies with the type of estuary and with differences in the spatial and temporal pattern of the community.
The lower abundance of fish in the rainy season may be related to the season of greater water volume in the river, providing greater availability of more sheltered areas, facilitating dispersal, and hindering fish collection. In estuarine environments, mangroves provide a natural refuge for young individuals due to the protection provided by the root structure of their trees. Most of the fish caught in tropical coastal areas enjoy this protection during their young phase and at the time of laying and thus depend closely on the integrity of this ecosystem (Lacerda, 1984). In general, the ichthyofauna remains with the most abundant species still well preserved, especially in the area further downstream from the river. For Teixeira et al. (2005), the determination of biodiversity, especially of the fish community and its spatial and temporal variation patterns, is of great relevance to assessing environmental quality.
The Siluriformes was the order with the most incredible abundance of fish in the Rio Guapi-Macacu. The dominance of Siluriformes over the others constitutes a characteristic pattern of the eastern region of Brazil, being particularly accentuated in areas of high river courses, where the condition of high hydrodynamics favors the occupation by demersal species (Bizerril & Primo, 2001). The site with the most increased occurrence of native species is also located downstream of the river, within Guanabara ESEC, the area of most preservation within the Guapimirim EPA and with better ecological indices, such as abundance and richness of the species found, especially in the dry season. Genidens genidens, representative of the second most abundant family, Ariidae, occurs in coastal areas and is generally more significant in shallow coastal waters, on a muddy or sandy bottom (Araujo, 1988; Andreata et al., 1989). The presence of G. genidens downstream of the river may be related to the spawning season. The species seek the mouth of the rivers performing oral incubation with males and rarely females, carrying eggs and initial forms of offspring until they complete embryonic development (Yanez-Arancibia & Sanchez-Gil 1988; Reis, 1986b), which explains the presence of specimens downstream in the Guapi-Macacu River. In addition, G. genidens had high levels of fidelity (59.09%) and specificity (100%), considered a perfect indicator species in the IndVal analysis. The IndVal method has some advantages compared to other bioindication methods, is calculated for each species independently, where the categorization of habitats occurs without restrictions and can be grouped subjectively or quantitatively (McGeoch & Chown, 1998).
Thus, the IndVal analysis establishes that for this specific area, regardless of the season analyzed, three species were considered indicators of this habitat G. genidens, B. pectinata, and M. furnieri (Figure 8A). In addition to these species, E. saurus was selected only for the dry season in the downstream area. All species chosen for the downstream area were considered asymmetric indicators, as they contribute more to habitat specificity than fidelity (Dufrêne & Legendre, 1997). This segment was also particularly evidenced in the cluster analysis, which showed that the main species selected in IndVal share this river segment.
The area within the Guapimirim EPA, disregarding the Guanabara ESEC (i.e., the intermediate segment of the river), revealed ecological indices similar to the other parts of the river. However, greater abundance and richness can be observed (Figure 8A). Thus, the downstream and intermediate segments (i.e., comprising Guanabara ESEC and EPA de Guapimirim) presented only C. undecimalis indicative of the EPA regardless of the time of the year approached (Figure 8A; 8B). Centropomus undecimalis belongs to the order Perciformes, the second most abundant in the Guapi-Macacu River. According to Peterson & Gilmore (1991), sea bass does not undergo large migratory cycles, being a relatively fast-growing fish that spawn a large number of eggs in brackish waters during late spring and early summer. Sea bass juveniles show a greater affinity for fresh water and survive in waters with lower oxygen levels than adults, being found upstream of rivers at all times of the year (Ager et al., 1976). Its primary or nursery habitat has been described as warm shallow streams or drainage channels, with low current and unvegetated bottoms or bordering the mangrove (Mcmichael et al., 1989). As they develop, they move from shallow water habitats to estuaries, mangroves, and deeper water (Tucker & Campbell, 1988). According to the cluster analysis, the river segment shared with C. undecimalis and other species provides this species with a habitat with abundant food resources and protection for its development.
The river's intermediate region was characterized by a very winding zone with greater diversity in physiography, constantly flooded with deeper portions, and a salinity gradient that decreases from the river's mouth towards the interior. This segment presents vegetation composed of mangrove forests, riverside types. This area is directly related to larger transparency samples, evidencing E. brasilianus and O. niloticus with intermediate values of this attribute (Figure 8B). Eugerres brasilianus is a species of marine origin that tolerates significant variations in salinity (Ramos et al., 2006), is anadromous, migrating from the sea to rivers, living in coastal waters of warm seas, penetrating coastal lagoons and estuaries to complete its life cycle (Yañez-Arancibia, 1986). In addition, E. brasilianus is a species with nocturnal habits, generalist and opportunistic; it is epibenthic and demersal. That is, it exhibits patterns strictly linked to the substrate, being did consider an excellent biological resource, mainly because it did regard as an abundant fishery resource (Cyrus & Blaber, 1983; Tapia-García & Ayala Pérez, 1996; 1997; Araújo & Santos, 1999; Barletta & Blaber, 2007; Barletta & Costa, 2009).
On the other hand, the cluster analysis did not evidence the intermediate region with a specific community for this segment of the river, showing itself as a transition area and occupied mainly by species that travel throughout the river, such as H. littorale, H. auroguttatus, and L. castaneus (Figure 8C). Hypostomus auroguttatus and L. castaneus belong to the most abundant family, Loricaridae, common in areas with muddy river bottoms and may even occur in lentic environments. That two species recorded in the three segments of the Guapi-Macacu River during the dry and wet seasons, considered generalists in the present study.
The species A. lacustris (Figure 5), considered rare in the analysis shown in CLAM TEST, was selected in IndVal for the upstream segment of the river, as well as in the rainy season, with high specificity and low fidelity, for Dufrêne & Legendre (1997), rare species may receive the same IndVal value as indicator species and are called asymmetric indicators. On the other hand, in this same river segment, without considering the attributes of the seasons (dry or wet), IndVal selected T. striatulus and C. gariepinus (Figure 8D), both with high specificity. Meaning that these fish can also be considered indicators asymmetric, which contribute to the specificity of the habitat, but they do not serve to predict groups (Dufrêne & Legendre, 1997).
From the CCA, we can see that the segment upstream of the river presents higher values of DO and abundance of C. gariepinus. The upstream part is the river's headwaters, which have a humid tropical climate, high and variable slope, determining the dynamic character of the fluvial system, with the presence of rapids, characteristic of mountain and plateau regions. Barella (2000) discusses the vital role of riparian forests in providing resources for feeding aquatic fauna and attracting dispersers, making the riparian environment a fundamental element in the sustainability of rivers and lakes and in the connection between the different systems that make up the rural landscape. The CCA also highlights the most protected area concerning the Guapimirim EPA, downstream of the river, with the most diversity and richness, exhibiting greater salinity, pH, and turbidity attributes. In general, the most abundant species in the river transit are intermediate values of the analyzed abiotic variables, except C. gariepinus, which correlates with larger samples of dissolved oxygen, and M. furnieri, which exhibits correlations with more significant correlations values of salinity. The species C. parallelus, H. auroguttatus, H. littorale, and L. castaneus express abundances related to intermediate values of transparency, revealing correlations in all river segments. Similarly to CCA, the cluster analysis also evidenced the group formed by G. genidens, B. pectinata, and M. furnieri, revealing sharing proximity in the same region, especially in the dry season, with the dominance of G. genidens, as it presents greater abundance in this group. The CCA also highlights the similar spatial distribution of T. striatulus with C. gariepinus (with more representation in abundance), corroborating the cluster analysis.
African catfish in the Guapi-Macacu River
The African catfish, C.gariepinus was the third most abundant in the river, however in the most preserved area of the Guapimirim EPA, it still does not show significant abundance. It also notices that the species that present ecological equivalence to the African catfish, R. quelen, and T. striatulus, despite showing a similar distribution, give a lower abundance, which denotes the habitat overlap of the IAS over the native ones (Figure 9A). In addition, the population of C. gariepinus exhibited greater abundance contributions in the dry season, especially upstream, compared to the other species, demonstrating a high potential to colonize the entire river (Figure 9B).
Even though the CCA analysis does not show similar correlations of the abiotic factors R. quelen with Clarias gariepinus, the group exposed in the cluster analysis, it is clear that these species share the same segments of the river. Rhamdia quelen prefers lakes and river bottoms, preferring calmer water environments with a sand and mud bottom along the banks and vegetation (Gomes et al., 2000). They are omnivores with a clear preference for fish, crustaceans, insects, plant remains, and organic debris (Guedes, 1980; Meurer & Zaniboni Filho, 1997). Therefore, they are considered a generalist about food choice (Guedes, 1980). Among the many biological similarities that R. quelen has with C. gariepinus, highlighting the food preference and the use of habitat, however R. quelen has a disadvantage about its development, since females can reach up to 66.5 cm and males up to 52.0 cm (Gomes et al., 2000).
According to our analysis, dissolved oxygen was the attribute directly correlated with the distribution of C. gariepinus (Figure 7B). Thus, dissolved oxygen (DO) plays a fundamental role in regulating the body's metabolic functions, including the aquaculture community, in addition to being an environmental indicator of water quality (Anyachor & Sikoki, in press). On the other hand, African catfish can withstand low concentrations of dissolved oxygen (Adewolu et al., 2008) due to an air-breathing accessory organ, which can absorb oxygen from the atmospheric air (Moussa 1956), allowing fish to survive for many hours or weeks out of water or in muddy swamps (Idahor et al., 2014). Thus, the most significant contribution of DO may have acted as a facilitator for the development of the IAS, serving as an attraction for other species that could migrate to this segment of the river, in search of better environmental conditions, and probably due to the greater dominance of the IAS, have failed to establish themselves in this area.
Another significant environmental attribute in our analysis was temperature, and this seems to be an essential factor in the distribution of the species in the Rio Guapi-Macacu. The highest temperature values in the upstream area corroborate the results found in the CCA, where the greatest abundance of the species did correlate with this segment of the river. For Hecht (2013), African catfish larvae exhibit an optimal development around 28ºC, whose value was recorded upstream in the rainy season. And this could be seen in the dry season, which showed a high increase in the IAS population, favored due to the temperature rise previously recorded. On the other hand, our studies indicate that, despite the average temperature values measured in the Guapi-Macacu River not being considered ideal for the development of catfish, the species' adaptability has allowed it to develop well in this ecosystem and colonize other segments of the river. However, climate changes resulting from global warming can contribute to the gradual increase in temperature, significantly altering this scenario, which may favor the rapid development of this alien species and, possibly, the decline of native populations.
Salinity is also an attribute that limits the occurrence of alien species in the mouth of Guanabara Bay. That is because African catfish are stenohaline, with a limited capacity to withstand increased salinity in the environment, in more advanced stages (Hoogendoorn, 1981). Borode et al. (2002) conducted a study of the effect of salinity on the early-stage development of African catfish. They concluded that increased salinity delays the hatching and development of African catfish eggs and larvae but accepts up to 6 ppt variations for its growth. De Melo et al. (2014) detected an intrusion of salinity into the river in the dry season of the year, corroborating our findings, where salinity varied considerably in this season, reaching 31.
Even so, we can observe that despite the significant abundance of this species, the analysis of specificity and fidelity does not list C. gariepinus as an indicator species, taking into account both studied seasons and collection areas. However, this pattern diverges when considering only the upstream zone, when the species specificity index rises to 81% and the fidelity to 36% for this area, demonstrating C. gariepinus with the probability of 53% being an asymmetric indicator species of this area. For Dufrêne & Legendre (1997), a species can be an asymmetric indicator without high fidelity.