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Introduction

In natural environments, the population viability of a fish species is entirely dependent on its capacity to adapt its reproductive tactics to the primary environmental conditions or the new conditions brought about by anthropic activities. Depending on the scenario, these tactics may not be enough to ensure a strategy that will maintain and perpetuate the species in the environment (Mérona, Mol, Vigouroux, & Chaves, 2009).

The reproductive tactics of fish are evaluated through multiple indicators, which are obtained from the morphophysiological and behavioral changes that occur in the populations, due to local and seasonal environmental conditions (Winemiller, 1989). The primary indicators used in reproduction studies reflect, for example, the level of investment in the production of gametes, spawning/spermiation or recruitment period (Brewer, Rabeni, & Papoulias, 2008), physiological condition of the animals, dislocation of fat for the incorporation of yolk in the ovarian follicles of females, and sexual maturation sizes of males and females (Brosset et al., 2016), among others.

Given the current scenario of multiple environmental impacts, many anthropic variables interfere with the homeostasis of the systems and, consequently, species fitness (Louiz, Ben-Attia, & Ben-Hassine, 2009), imposing an adaptive pressure on the reproductive tactics in order to ensure population viability. In this context, pollution is one of the many impacts faced by native species (Yamamoto et al., 2016), in addition to the changes in watercourses that generally occur as a result of dams (Weber et al., 2013; De Fries, Rosa, Silva, Vilella, & Becker, 2018).

The Lower Iguaçu River region is a critical example of these impacts since its course is interrupted by six hydroelectric power plants (HPP), five of which are currently in full operation. On the other hand, the ichthyofauna of the Iguaçu River is considered one of the most singular in the world, with more than 75% endemic species (Baumgartner et al., 2012). The scenario suggests a significant, long-term issue related to the global extinction of species, demanding efficient biological indicators in order to detect changes in the structure of fish assemblages.

In the search for ideal biological indicators, it should be noted that not all species respond negatively to dams (e.g. population decreases/endangerment). There are generalists, or so-called explorer species, with great adaptive capacity, which use the new conditions to reconfigure their reproductive tactics and reach their biotic potential (r_max), mediated by resource availability and spawning sites and by the inexistent/low control of the trophic chain (bottom-up and top-down), especially during the first years of flooding (Mérona, Vigouroux, & Horeau, 2003; Silva, Muelbert, Oliveira, & Favaro, 2010).

The fish species Astyanax bifasciatus (Garavello & Sampaio, 2010) is popularly known as the red-tail lambari and is restricted to the Iguaçu River Basin; therefore, it is considered endemic to the region. Astyanax bifasciatus is a generalist species that has drastically increased its fitness in artificial lakes due to the dams (Silva et al., 2010), demanding the monitoring of its auto-ecology in tributaries to generate data that allow its management or use as bioindicators.

Thus, this study sought to evaluate the reproductive biology of the endemic species A. bifasciatus in a tributary of the Lower Iguaçu River Basin, Paraná, Brazil.

Material and methods

Study area

This study was conducted in four sampling points (P1 to P4) along Jirau Alto River, in the city of Dois Vizinhos, southwestern Paraná, Brazil (Figure 1). The Jirau Alto is a second-order river, a tributary of the Dois Vizinhos River, sub-basin of the Chopim River, which is one of the three most important rivers of the Lower Iguaçu River Basin (Pigosso, Bonfante, Farias, Becegato, & Onofre, 2009).

P1 was situated near the headwaters of the Jirau Alto River, with denser riparian vegetation that undergoes periodic flooding. The river is about one meter deep here and the riverbed is muddy (fine sediment). P2 was established approximately 3 km downstream. It is an area with scarce riparian vegetation and a deeper riverbed (1.5 m) with fine sediment. The other points were about 1.5 km from each other. Dense riparian vegetation similar to P1 was verified in P3. In P3, like P4, the river presented greater velocity and its bed was composed of gravel and coarser sediment. P4 was located near the mouth of the Jirau Alto River and its riparian vegetation was restricted to 5 m from the riverbank.

The city of Dois Vizinhos has an area of 418 km², an average altitude of 509 m, and is located between the geographical coordinates 25°44’35’’ S and 53°4’30’’ W. Its vegetation is classified as ecotonal, between Semideciduous Seasonal Forest and Mixed Ombrophilous Forest, both presenting phytophysiognomies of the Atlantic Forest (Instituto Brasileiro de Geografia e Estatística [IBGE], 2004).

The climate of the region is characterized as Cfa; humid subtropical mesothermal with hot summers, an undefined dry season, and an average temperature of the coldest and hottest months below 18ºC and above 24ºC, respectively. Frosts are infrequent and the winds are predominantly south-southeast during mild weather and north-northeast in rainy periods (Maack, 1981). Relative air humidity ranges from 70 to 75% and rainfall is between 1,800 and 2,200 mm year^-1 (Nitsche, Caramori, Ricce, & Pinto, 2019).

Sampling and laboratory procedures

We performed monthly standardized collections during the full moon from October 2015 to September 2016. The full moon was chosen because there is accumulated experimental evidence that fish from tropical and subtropical waters use moonlight-related periodicities as reliable information for synchronizing the timing of reproductive events (see Ikegami, Takeuchi, Hur, & Takemura, 2014 for more information).

Fish were captured using a set of three gill nets (15, 20 and 25 mm mesh sizes between opposite knots, 10 m long and 2.0 m high). A fish trap was also used (80 cm long and 40 cm in diameter) at each sampling site. The nets were arranged parallel to the riverbank and the fish traps were placed in deeper areas or where there was marginal vegetation. Both types of fishing gear were immersed in water for 24 hours at each site. The set up and removal of the fishing gear were always carried out early in the morning on the same day at all sampling sites.

The captured fish were anesthetized and euthanized using 250 mg L^-1 benzocaine hydrochloride, according to the CONCEA Directives for Euthanasia Practice, which regulates the procedures and methods of euthanasia in animals (Conselho Nacional de Controle de Experimentação Animal [CONCEA], 2018). The fish were later refrigerated and transported to the Zoology lab of the Universidade Tecnológica Federal do Paraná (UTFPR), Dois Vizinhos Campus, for processing.

Authorization to collect the fish was obtained from SISBIO under protocol nº 50414-1. The study was previously approved by the UTFPR Ethical Committee on the Use of Animals, under protocol nº 2015-20.

The taxonomic identification of the fish was confirmed in the laboratory (Baumgartner et al., 2012). Morphometric measurements for total (Lt) and standard (Ls) length (cm) and total weight (Wt) (g) were subsequently determined. The animals were than sectioned to expose the viscera. The liver and gonads were removed and weighed using a semi-analytical balance. Individuals with somatic fat were only counted for frequency estimates.

Before removing the gonads from the abdominal cavity, a previous macroscopic analysis was performed to identify the sex and outline the stage of ovarian and testicular development, as proposed by Bomfim, Peretti, Camillo, Costa, and Nascimento (2015).

Endpoints and Data Analysis

The parameters used to evaluate the reproductive cycle of A. bifasciatus were: sex ratio, gonadosomatic index, frequency of gonadal development stages, frequency of individuals with celomatic fat, hepatosomatic index, total and somatic condition factor (allometric model), and sexual maturation length.

The sex ratio was analyzed applying the G-test, evaluating the difference as regards the expected proportion (1:1) of female and males. The results were considered significant when p < 0.05.

The individual gonadosomatic index (GSI) was used to calculate the monthly average GSI, which was used to elaborate the maturation curve for females and males. The GSI was obtained by equation 1 (Araújo, Morado, Parente, Paumgartten, & Gomes, 2018):

where:

Wg = weight of the gonad;

Wt = total weight of the individual.

The percentage frequency of gonadal developmental stages was determined for separate sexes. The developmental stages were initially identified as: immature (IMT); maturing (MTG); mature (MAT); spawned or recovered (females)/spermiation or emptied (males) (SPN). The monthly percentage of the stages was calculated later, considering the separate sexes.

Only females were used to analyze the frequency of individuals with celomatic fat and the hepatosomatic index because of their ability to incorporate yolk into the ovarian follicles during the reproductive process, which affects their ability to accumulate fat and later make it available. The hepatosomatic index (HIS) was estimated individually and the monthly average HSI was subsequently calculated. The HSI was obtained by equation 2 (Araújo et al., 2018):

where:

Wl = weight of the liver;

Wt = total weight of the individual.

To correlate the allocation of resources with the reproductive process, the allometric condition factor was calculated for both sexes. The condition factor was determined monthly and for the separate sexes (Lima-Junior, Cardone, & Goitein, 2002) using the total (K) and somatic (K') condition factor. The calculations were performed based on equation 3 (Vazzoler, 1996):

where:

Wt = total weight – used to calculate K;

Ws = somatic weight (disregarding the weight of the gonad) – used in K’;

Ls = standard length;

b = angular coefficient obtained through the weight-length relationship using the minimum square method, as described by Le Cren (1951).

First maturation size is an estimate based on length classes and the frequency of adults in the population. This analysis generally seeks to estimate the length at which 50% of the population (L₅₀) are adults. The standard length of the individuals was used for this study, which considered adults to be those with gonads in the maturing, mature or spawned/spermiated stage.

The L₅₀ were estimated separately for females and males using a curve that correlates the relative frequency of adult individuals with the midpoint of the length classes obtained through the Sturges Postulate. The model used to adjust the curve was expressed by equation 4 (Lemos, Varela-Junior, Velasco, & Vieira, 2011):

where:

Fr = relative frequency of adult individuals;

e = base of the Napierian logarithm;

a = intercept value;

b = angular coefficient obtained using the least squares method;

Lp = midpoint of the length classes.

Results

A total of 160 individuals were collected (104 females and 56 males) (Table 1). The prevalence of females occurred throughout the entire collection period, but no significant difference was observed (G test = 15.51; p = 0.16; df = 11).

The maturation curve (Figure 2) demonstrated that, for females, the highest average GSI values occurred in October and November, followed by an abrupt decrease in January and February. A new increase in the GSI between March and May (smaller) was subsequently verified, indicating a long reproductive period with two investment cycles. A progressive increase occurred in the GSI values in later months, suggesting maturation.

Male and female gonadal development were similar, with the highest GSI values occurring from August to December, followed by a sudden decline in January and February. Males also appear to have a second investment cycle between March and June. In subsequent months, there was a progressive increase in gonadal development.

The monthly frequency of the gonadal maturation stages of females and males (Figure 3) complements the previously reported GSI results, demonstrating a higher proportion of mature female individuals from September to January and males from October to December. The second period of frequencies of mature individuals was from March to July for males, except in April (no mature males). There was a reduction in the frequency of mature females in February, followed by a new increase from March to May.

Immature individuals were present in February, April, and July, indicating a potencial recruitment and reinforcement of the second reproductive period of the year. There was a higher proportion of females in the spawning stage from December to February and May to June. As regards the males, there was a continuum of spermiated individuals from January to May.

In general, individuals in maturation were observed from June to December for both sexes, with a progressive increase in their number, corroborating the GSI increase during the period.

Based on the frequency of females with celomatic fat, the lowest values were observed from September to October, intermediate values from November to April, and the highest values from May to August. This information agrees with the average hepatosomatic index (HSI) values, which regress during the period in which there are individuals with greater fat accumulation (Figure 4). On the other hand, the highest values of HSI were observed in September, April and May, indicating fat metabolism for the reproductive cycle.

The condition factor showed that females and males present two periods with the highest average K values throughout the year, from June to September and from February to March. After both periods, a decrease in K values was verified. Moreover, the most relevant differences between K and K' for both sexes were found to have occurred between July and December, suggesting a higher investment in the gonad (Figure 5). These results are consistent with the GSI and frequency of gonadal maturation stages.

Length at first sexual maturity (L⁵⁰) was estimated to be 4.57 cm for females and 3.56 cm for males. The shortest length at which all individuals were fit for reproduction (L₁₀₀) was estimated to be 8.36 cm for females and 9.53 cm for males (Figure 6).

Discussion

The reproductive indicators used in this study were sensitive and responsive, and showed morphophysiological changes that occurred in A. bifasciatus individuals collected for one year in the Jirau Alto River, a tributary of the Lower Iguaçu River Basin. The coordination of responses observed from the gonadal development, accumulation and availability of celomatic fat, liver biomass, and physiological status of the individuals support the arguments of the present authors concerning the reproductive tactics adopted by the species for its maintenance in this environment.

The relationship between the GSI indicators and the percentage frequency of the gonadal maturation stages indicated the existence of a long reproductive period, suggesting parceled spawning. This type of spawning has been histologically documented for species in older reservoirs of the Upper Iguaçu River Basin, which shows greater environmental stability (Silva et al., 2010). On the other hand, according to the same authors, species in newly formed reservoirs, the species adopted total spawning as a reproductive tactic, which was related to a more favorable period of the year. In the present study, the species used an adapted reproductive tactic, with two cycles of major investment throughout the year, demonstrating its great adaptative capacity (Abilhoa & Agostinho, 2007), according to the environmental scenario in which it is inserted.

In general, species of the Astyanax genus exhibit a long reproductive period and large investments in small and numerous oocytes (Agostinho et al., 1999). However, not all species of this genus have the same adaptive plasticity, due to the variations observed in their ecomorphological attributes and diet composition (Mise, Fugi, Pagotto, & Goulart, 2013). Astyanax minor, for example, has a higher colonization capacity in newly formed reservoirs (Oliveira, Santos, Fávaro, & Abilhoa, 2008). This is due to its detritivorous diet and its high capacity to produce numerous and small oocytes, as well as presenting one of the highest fecundities and gonadosomatic relationships observed for the Astyanax genus in the Iguaçu River. In older reservoirs, undergoing environmental rebalancing, the species decreases its dominance and yields to the predominance of Astyanax bifasciatus, which presents intermediate reproductive characteristics (Bailly, Agostinho, Suzuki, & Luiz, 2005) and a herbivorous or omnivorous diet.

In fact, A. bifasciatus has been more successful in 20 to 40-year-old reservoirs in the Iguaçu River (Daga & Gubiani, 2012) and have presented intense and wide reproductive activity, with many spawnings throughout the year, as mentioned above. The oocytes of this species are larger than those of A. minor and are produced in smaller quantities (Bailly et al., 2005). On the other hand, the larger size of A. bifasciatus (Abilhoa & Agostinho, 2007; Gubiani & Horlando, 2014) compensates, in part, for the production of gametes and favors the swimming performance of the animals (Mise et al., 2013), helping them deal with top-down control and the search for allochthonous food. Thus, A. bifasciatus uses a set of reproductive tactics in newly-flooded reservoir environments, with higher productivity and strong environmental fluctuations. Other tactics are adopted in older environments undergoing community rebalancing, where interaction with other species becomes an important variable.

Another coneger species endemic to the Iguaçu River is Astyanax gymnodontus, which is worth comparing to A. bifasciatus. The characteristics of A. gymnodontus are more demanding than the other species of Astyanax mentioned, having lower fecundity, larger oocytes (Bailly et al., 2005), larger body size, later first maturity (Baumgartner, Silva, & Baumgartner, 2016) and an insectivorous diet with herbivorous tendencies (Cassemiro, Hanh, & Delariva, 2005). The species is relatively successful and abundant in older reservoirs. Nevertheless, community dominance in these environments is always exercised by A. bifasciatus (Daga & Gubiani, 2012), probably due to its intermediate ecomorphological characteristics that favor greater resilience.

In natural environments, such as streams, species would be expected to have adapted to the natural disturbance events and, therefore, would have responded similarly in older reservoirs. This presumption is partially correct since mature individuals are found throughout most of the year. However, the GSI values showed two periods of higher reproductive intensity. This investment in two reproductive seasons is probably related to the intensity of the disturbances, whether originating from natural processes or related to different anthropic activities. In addition to the construction of dams, changes in the habitat/landscape structure, such as the observed suppression of riparian vegetation in the Jirau Alto River (Pigosso et al., 2009), might intensify the effect of floods, making conditions unfavorable for reproduction (Franssen et al., 2006; De Fries et al., 2018). This environment can become more susceptible to the influx effects of urban, industrial or agricultural contaminants, as observed in the Jirau Alto River (Wachtel et al., 2019) and other tributaries of the Lower Iguaçu River Basin (Nimet, Amorim, & Delariva, 2018).

Immature individuals of both sexes were also recorded for a long period in the study area (February to July), suggesting their use in recruitment. This demonstrated the importance of the study area for the entire life cycle of the species, from hatching and larval development to adulthood with gonad maturation and spawning/spermiation. As a species endemic to the Iguaçu River Basin, but with previously-mentioned r-strategist characteristics, it is essential to conserve the habitat and landscape structure to maintain the characteristics of the entire community, controlling species such as A. bifasciatus, which presents high biotic potential. A potential indirect effect derived from the population growth of generalist species is their population increase in tributaries (colonization and recolonization), which can cause an increase in interspecific competition and changes in the structure of fish assemblages (Araújo et al., 2013). The species can act as a natural indicator of community vulnerability, responding to changes in the habitat of the Iguaçu River and its tributaries. This positive relationship, due to landscape destructuring in the Iguaçu River Basin, was recently reported by Delariva et al. (2018) and can be used for bioindication (Bueno-Krawczyk et al., 2015; Nimet et al., 2018).

All analyses presented and discussed in this study corroborate the results obtained for the total condition factor (K) of the species. The most significant difference between K and K' in both sexes was consistent with periods of greater gonadal investment and high frequency of mature individuals. The progressive decrease in K values in the subsequent months supports the argument for spawning and spermiation intensification, leading to nutritional stress (Querol, Querol, & Gomes, 2002), due to the physiological changes resulting from the energetic reallocation. Thus, the species accumulated celomatic fat in the fall and winter, and spent it in the early spring with maturation, which precedes the peak of reproductive activity. A sudden HSI increase in the early spring was also observed, suggesting the displacement of the energy reserves to the gonads for storage, as reported by Abelha and Goulart (2008). The pre- and post-spawning/spermiation periods showed animals with the best nutritional conditions, as observed for other species of the genus (Hirt, Araya, & Flores, 2011; Viana, Tondato, Súarez, & Lima-Junior, 2014), indicating the physiological preparation/recovery of the animals for the reproductive process. In this case the variations in K were well-synchronized to the reproductive process, although the relationship is not always linear or exclusive. The physiological condition of the animals is modulated by other factors, such as fluctuations in environmental parameters, food availability, interspecific relationships (parasitism), anthropic pressures and ontogenetic variations (Le Cren, 1951; Datta, Kaur, Dhawan, & Jassal, 2013).

Length at first maturity (L₅₀) showed that the species has a strong generalist characteristic, with rapid growth and maturation of its gonads. Even small individuals (3.5 to 4.5 cm) participate in the reproductive process, even smaller than those already reported for the species in Iguaçu reservoirs (Baumgartner et al., 2012). This divergence is probably associated with the type of environment and intensity of the disturbances. The species submitted to running water environments, with frequent floods associated with habitat degradation and pollution, as observed in the Jirau Alto River, probably presents accelerated sexual maturity as another tactic that aims to ensure reproductive success and its maintenance in the environment. The sexual maturity of females that were larger than males also seems to be a tendency for other abundant endemic Astyanax species from the Iguaçu River, such as A. dissimilis (Suzuki & Agostinho, 1997), A. gymnodontus (Baumgartner et al., 2016) and A. minor (Baumgartner et al., 2012). The present study suggests that the divergence in resource allocation between the sexes and the sexual selection process act as the main adaptive forces, making this indicator an important tool to evaluate sexual dimorphism in the genus.

Conclusion

The use of multiple reproductive indicators has allowed a more thorough and integrated view of the reproductive process and techniques adopted by the endemic colonizer, Astyanax bifasciatus, in a small tributary of the Lower Iguaçu Basin. The results encourage the adoption of conservationist strategies for the tributaries in the region, with the aim to manage the species as an indicator of habitat changes.

Acknowledgements

This study was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq - Brazil), Fundação Araucária and Universidade Tecnológica Federal do Paraná.

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