Marcilene Lima-Lima1 
, Nathalia C. López-Rodríguez2, Elane Guerreiro Giese3 and Bruno da Silveira Prudente4
PDF: EN XML: EN | Supplementary: S1 S2 | Cite this article
Abstract
Este estudo descreve a história de vida de Pyrrhulina capim em riachos da Amazônia Oriental, indicando os principais preditores ambientais que influenciam sua atividade reprodutiva. Os espécimes foram coletados entre março de 2019 e março de 2020 em uma bacia hidrográfica da bacia do rio Guamá. A população de P. capim foi avaliada através da proporção sexual, comprimento na primeira maturação (L50), atividade de maturação gonadal, padrão de crescimento, tipo de desova e fecundidade. Os efeitos das variáveis ambientais na atividade reprodutiva foram analisados separadamente por sexo usando Regressão Linear Múltipla (MLR). Um total de 404 indivíduos foram analisados, compreendendo 218 fêmeas e 186 machos, sem diferenças significativas na proporção sexual. As fêmeas atingiram a primeira maturação em 24,91 mm, enquanto que para os machos, esse comprimento foi de 21,47 mm. A atividade reprodutiva foi consistente em ambos os sexos durante todo o período de estudo. A espécie exibiu crescimento alométrico positivo (b = 3,12) sem diferenças notáveis entre machos e fêmeas. O diâmetro dos ovócitos variou de 0,05 mm a 0,70 mm, indicando desova em lotes múltiplos. A fecundidade média foi de 162 ovos. A largura do riacho, a profundidade e o tipo de substrato foram responsáveis por 13% da variabilidade na atividade reprodutiva feminina. Estes resultados sugerem que P. capim possui uma estratégia reprodutiva oportunista.
Palavras-chave: Desova, Fecundidade, Maturação sexual, Precipitação.
Introduction
Life history theory attempts to understand how the phenotypes of organisms are designed throughout their life cycle and how they are influenced by intrinsic and extrinsic factors, such as behavior and environmental conditions, respectively (Stearns, 2000). Reproductive strategies and tactics are considered one of the most important life history traits, as they contribute to population maintenance under specific environmental conditions (Vazzoler, 1996; Caramaschi, Brito, 2021). According to Gross (1996), reproductive strategies result from the somatic and reproductive efforts of an organism, which are genetically defined in an evolutionary context. In contrast, reproductive tactics are strongly influenced by local environmental conditions, although they operate within a range defined by the organism’s strategy (Gross, 1996).
Teleost fish exhibit the highest diversity of reproductive strategies and tactics among vertebrates (Helfman et al., 2009). Species experiencing similar environmental conditions may develop comparable reproductive tactics, whereas individuals of the same species may have different tactics when subjected to distinct environmental conditions (Althoff et al., 2024). Fish life history is strongly associated with environmental changes, whether natural or anthropogenic (Becker et al., 2008). In temperate streams, temperature and photoperiod are the main environmental predictors of fish reproductive tactics (Migaud et al., 2010). However, in the tropical regions, where temperature and photoperiod are relatively stable, rainfall becomes the primary environmental driver of life history traits in stream fish species (Kramer, 1978; Caramaschi et al., 2021).
Streams are small watercourses with unidirectional flows, and unstable beds (Townsend et al., 2010). In this system, geomorphological and lithological features shape their sinuosity and influence physicalchemical conditions of water, such as hydrogen potential, dissolved oxygen, and electrical conductivity (Sioli, 1957; Araújo-Lima et al., 1995). The small dimensions of streams also make these systems heavily dependent on riparian vegetation (Teresa, Casatti, 2010), that supports primary productivity and provides microhabitats for fish reproduction and growth (Kiffney et al., 2004; Graziano et al., 2022).
Stream fishes are predominantly small bodied (Buckup, 2021), which makes many of these species popular in the aquarium market (Weitzman, Weitzman, 2003) rather than targets for subsistence or commercial fishing. Therefore, studies on the reproductive biology of these species in natural environments are limited compared to those on larger species fish used for human consumption. Most research on small fish reproduction have been restricted to experimental studies under controlled conditions (Cacho et al., 2006; Moorhead, Zeng, 2010; Kodama et al., 2011). A small portion of these studies have addressed the ecological role of these species and their participation in ecosystem processes in nature habitats (López-Rodríguez et al., 2021; Oliveira et al., 2023).
Among tropical stream fishes, some species from the Lebiasinidae family show high abundance and strong association with microhabitats provided by riparian vegetation (Silva et al., 2010; Kemenes, Forsberg, 2014; Prudente et al., 2017; Santos et al., 2022). Many species in this family have an omnivorous eating habit, consuming items of allochthonous material drifting on the water surface (Silva, 1993; Arias, Rossi, 2005; Brejão et al., 2013). These species are distributed across most of South America, excluding Chile (Weitzman, Weitzman, 2003), preferably inhabiting backwaters along rivers and streams margins (Sabino, Zuanon, 1998). Many lebiasinids also have vivid colorations, which makes them even more popular in the aquarium trade (Weitzman, Weitzman, 2003).
Currently, 74 species are recognized in the family Lebiasinidae, allocated among the genera Copeina Fowler, 1906, Copella Myers, 1956, Derhamia Géry & Zarske, 2002, Lebiasina Valenciennes, 1847, Nannostomus Günther, 1872, and Pyrrhulina Valenciennes, 1846 (Fricke et al., 2025). These species have small body size, with adult reaching a maximum standard length of approximately 16 mm in species such as Nannostomus anduzei Fernades & Witzman, 1987, and approximately 200 mm in Lebiasina species (Queiroz et al., 2013). They display a variety of reproductive strategies closely tied to environmental conditions (Cordeiro et al., 2022; Althoff et al., 2024). For instance, Copella arnoldi (Regan, 1912) deposits its gametes on leaves outside the water, with males keeping the eggs moist by continuously spraying water until hatching (Krekorian, Dunham, 1972).
Within this family, Pyrrhulina capim Vieira & Netto-Ferreira, 2019 popularly known as pencil fish, is widely distributed across Eastern Amazon drainages, including coastal basins of the Amazon estuary (Vieira, Netto-Ferreira, 2019). This species preferentially inhabits low-order streams, with clear waters, sandy substrates and submerged vegetation (Vieira, Netto-Ferreira, 2019). This species has marked sexual dimorphism in the adult phase, with males displaying dark spots on the distal margins of their anal and pelvic fins and a higher number of maxillary teeth compared to females (Vieira, Netto-Ferreira, 2019).
The study aimed to characterize the reproductive strategy of P. capim based on novel information we collected on their reproductive tactics in streams of the Eastern Amazon and to identify key environmental factors that predict its reproductive activity. We hypothesize that P. capim follows an opportunistic reproductive strategy, combining tactics common of small fish, such as batch spawning, low fecundity, and early maturation (Winemiller, Rose, 1992). Additionally, we expect greater intensity of reproductive activity in months of higher precipitation, which enhance food resources availability and provide favorable microhabitats for juvenile development (Kramer, 1978; Abelha et al., 2001; Viana et al., 2006).
Material and methods
Study area. This study was conducted in two low-order streams (1st to 2nd order sensu Strahler, 1957) with similar physical habitat characteristics. These streams sampled monthly from March 2019 to March 2020. The streams are located in a 1,240-ha catchment area on the left bank of the Guamá River, within the municipality of Capitão Poço, in the state of Pará, Brazil (Fig. 1). The region has a humid tropical climate classified as Af in the Köppen system, as modified by Peel et al. (2007). Average annual rainfall is 2,370 mm, with the rainy season occurring from January to May and the dry season from August to November (INMET, 2021; Oliveira et al., 2023). The average monthly precipitation in the driest months is approximately 45 mm, while in the rainiest months, it reaches around 400 mm (Silva et al., 1999; Pacheco, Bastos, 2001).
FIGURE 1| Geographic location of the Capitão Poço River microbasin, Guamá River basin, Capitão Poço municipality, State of Pará, Brazil. The black circles represent the streams where specimens of Pyrrhulina capim were sampled.
The local vegetation is classified as equatorial sub-perennial forest (IBGE, 1992). However, the current landscape of the study area is primarily characterized by agricultural land and cattle pastures (Pacheco, Bastos, 2001), with isolated patches of secondary (Silva et al., 1999) and riparian forests. These riparian areas are protected as permanent preservation zones under the Brazilian Forest Code (federal law number 12.651/2012) (Rodrigues et al., 2016).
Data collection and analysis. In each stream, we defined a 50-m stretch divided by six cross-sections, resulting in five 10-m longitudinal sections where environmental conditions were measured, and fish species were sampled. Water physicochemical features, including dissolved oxygen (%), electrical conductivity (μS/cm-1), pH, and temperature (°C), were measured using a multiparameter device (ASKO, model AK88). Stream flow speed (FS, m/s) was recorded at three equidistant points in a cross section using the time taken for a floating object to travel a known distance. This data was then used to calculate the stream discharge (m3/s) using the equation Q =A × Vm, where A is the average transect area and Vm is the mean flow speed. The mean transect area was calculated as ΣAn = [(Z₁ + Z₂) / 2]) * w + [(Z₂ + Z₃ ) / 2]) * w + … [(Zn + Zn₊₁) / 2]) * w, where Zn is the measured depth of each equidistant point and w is the width of these three points.
At each cross-section, we measured the average channel width (WW, m), thalweg depth (TD, cm), and the percentage of substrate types. These parameters were assessed following the Standardized Protocol of the Igarapés Project (Mendonça et al., 2005). Average channel width was measured with a graduated pole, and average channel depth was measured at five equidistant points (left margin, left center, center, right center, and right margin) along each cross-section. Substrate composition was visually estimated at the same cross-sections, including silt (< 0.06 mm), sand (0.06 to 2 mm), fine gravel (2 to 16 mm), coarse gravel (16 to 64 mm), wood, roots, organic matter, leaf bank, and macrophytes. Monthly rainfall data were obtained from the Instituto Nacional de Meteorologia (INMET, 2021, Station A248, Capitão Poço).
Specimens of P. capim were collected from each 10-meter section using rectangular sieves (80 cm × 60 cm, 2 mm mesh) over a 12 min by a three-person team. Specimens were euthanized with eugenol (6 ml / 3 L of water), fixed in 4% formalin solution for approximately 48 h, and preserved in 70% ethanol. Voucher specimens were deposited in the Ichthyological Collection of the Aquatic Ecology Group (GEA), Universidade Federal do Pará, Belém (UFPA), under catalog number GEA.ICT 12065.
In the laboratory, specimens were measured for their total weight (Wt) using an analytical balance with a precision of 0.0001g, and standard length (Ls) using a caliper with 0.01 mm precision. Gonads were removed, weighed (Wg, precision: 0.0001 g) and preserved in 70% alcohol. Then, sex and maturation stages were previously evaluated under a stereomicroscope (Olympus, model CX21 and with 32x magnification) following Núñez, Duponchelle (2009), using morphological. Undetermined gonads were subjected to histological analysis, following Prophet et al. (1995).
The microscopic definition of the maturation stages was based on the presence and frequency of cells from the spermatogenic and oogenic lineages according to the classification suggested by Núñez, Duponchelle (2009). Females were classified into five gonadal stages: 1) immature, characterized by the predominance of previtellogenic oocytes (stage I), which present a basophilic homogenous ooplasm, large central nuclei with central or sub-central nucleoli, and a high nucleoplasmic ratio; 2) maturing: characterized by the presence of previtellogenic oocytes (stage I), with a predominance of oocyte in early vitellogenesis (stage II). The latter is distinguished from stage I oocytes by the presence of cortical alveoli. Oocytes in advanced vitellogenesis (stage III) can also be observed at this stage of gonadal maturation, which is characterized by the presence of the chorion being clearly visible, follicular cells and the theca generally well developed; the nucleus or germinal vesicle is still visible and located in a central position; 3) mature: characterized by the predominance of stage IV oocytes, which are characterized by cytoplasm filled with large yolk globules. Previtelogenic (stage I) and early vitellogenic (stage II) oocytes were also observed at a low frequency during this stage of gonadal maturation; 4) spawned: characterized by the presence of previtellogenic oocytes (stage I) and new batches of vitellogenic oocytes (stage II and III), which makes the ovary partially filled. Post-ovulatory follicles and some atretic oocytes were also found in this gonadal maturation stage; 5) resting: It presents characteristics like those of an immature female, with a predominance of previtellogenic oocytes (stage I), distinguishing it from this gonadal stage by the presence of a thicker ovarian wall. Some atretic follicles were also observed in this gonadal stage.
Males were classified into four stages: 1) immature, characterized by the presence of undifferentiated germ cells and spermatogonia surrounded by a large amount of connective tissue; 2) maturing, characterized by the presence of spermatogonia located along the seminiferous tubules, spermatocytes, spermatids, and a small amount of spermatozoids; 3) mature, characterized by the presence of a large number of spermatozoids in the lumen of the tubule; and 4) spent, characterized by the presence of practically empty seminiferous tubules and a few residual spermatozoids.
The sex ratio of P. capim was assessed for the whole study period as well as for each month. Differences in this sex ratio were analyzed using the Chi-square (χ²) test of goodness-of-fit, with the null hypothesis stating that the population’s sex ratio does not differ from 1:1, as proposed by Vazzoler (1996).
The mean length at which 50% of the population reached sexual maturity (L50) was determined separately for males and females using the logistic equation , where P represents the proportion of adult individuals, A is the proportionality coefficient, r is the rate of phase change from juveniles to adults, Ls is the standard length in mm, and L50 is the mean length at which 50% of the population attains sexual maturity. For this analysis, a length class with a 2 mm range was defined. Both the equations were fitted using the Solver routine in Microsoft Office Excel® 2016.
The reproductive activity of the P. capim population was assessed using the Gonadosomatic Index (GSI) and variation in the frequency of maturation stages throughout the sampling period. The GSI was calculated using the formula GSI = (Wg / Wt) * 100, where Wg represents the gonad weight and Wt is the individual’s total weight. GSI values were tested for normality and homoscedasticity, and their variation across the sampled months was analyzed using the non-parametric Kruskal-Wallis test (Kruskal, Wallis, 1952), followed by a Wilcoxon multiple comparison test (Wilcoxon, 1945). This analysis was conducted separately for males and females, excluding the immature specimens.
The growth pattern of P. capim was assessed through the weight-length relationships of individuals, following the model proposed by Järvi (1920) (see Froese, 2006), expressed by the equation, where Wt represents the individual total weight, Ls is the individual standard length, a is the proportionality coefficient, and b is the allometric coefficient. This equation was fitted using the Solver routine in Microsoft Office Excel® 2016. To test for potential differences in growth patterns between sexes, the residuals of this relationship were examined for normality and homoscedasticity and then compared between males and females using the Mann-Whitney U test.
The spawning type and fecundity of P. capim were determined by examining seven mature gonads. The spawning type was classified based on the frequency distribution of oocyte diameters, measured macroscopically, and confirmed through analysis of the occurrence of different oocyte development stages in histological sections. Oocytes were manually dissociated and photographed using a Motic stereomicroscope, model BA310E (40x magnification), equipped with a camera. Oocyte diameters were measured using the ImageJ® software, with a spherical object of known diameter serving as a reference. Fecundity was estimated based on the number of vitellogenic oocytes, defined as oocytes in stage IV of maturation (Núñez, Duponchelle, 2009). Macroscopically, vitellogenic oocytes were distinguished by their larger size, fuller appearance, and yellowish color. Oocyte counts were performed under a stereomicroscope at 40x magnification.
To assess the influence of environmental variables on reproductive activity of P. capim, a Multiple Linear Regression (MLR) model was applied, using the Gonadosomatic Index (GSI) as response variable. Variable selection was based on ability to predict GSI variation was conducted using the Akaike Information Criterion (AIC) (Zuur et al., 2009), which the lowest AIC value represented the best-fit model to predict the relationships between reproductive activity and environmental variables. The analysis was performed separately for males and females, with a significance level of 5%, using the MuMIn (Bartoń, 2020), Car (Fox, Weisberg, 2019) and Vegan (Oksanen et al., 2020) packages of R software (version 4.1.1).
Results
The streams presented an average pH of 5.59 (standard deviation = ±0.78), a temperature of 26.18 °C (±0.83), dissolved oxygen of 56.03% (±27.69), and electrical conductivity of 20.46 μS/cm-1(±3.10). Regarding the channel morphology, the streams exhibited an average wetted width of 3.05 m (±1.68), a talweg depth of 44.05 cm (± 6.05), and a flow velocity of 0.16 m/s (± 0.06). The average stream discharge was 0.14 m3/s (± 0.08). The substrate was predominantly composed of leaf banks (48.08%), followed by roots (11.86%), sand (9.46%), silt (8.56%), wood (6.73%), fine gravel (6.68%), coarse gravel (5.29%), and organic matter (2.93%). Rainfall peaked in February (511.6 mm) and was the lowest in September (34 mm).
A total of 404 specimens were evaluated, 218 females and 186 males. Of these 254 individuals were macroscopically examined to determine sex and sexual maturation stages, and 150 underwent histological procedures for confirmation. Females present an average standard length (Ls) of 24.94 mm (maximum of 53.69 mm and minimum of 10.56 mm) and an average total mass (Mt) of 0.34 g (maximum of 2.61 g and minimum of 0.01 g). Males had an average Ls of 24.97 mm (57.57 – 9.87 mm), and an average Mt of 0.38 g (2.92 – 0.01 g).
The proportion of males and females of P. capim did not differ throughout the study period (χ2 = 2.5; gl = 2; p = 0.08). However, in September, a difference in the sex ratio were recorded (χ2 = 10.8; df = 2; p = 0.001), with four females for every male (Fig. 2).
FIGURE 2| Sex ratio of males and females of Pyrrhulina capim sampled from March 2019 to March 2020 in the Guamá River basin, Eastern Amazon, State of Pará, Brazil. The asterisk indicates a significant difference in sex ratio. The dashed black line represents the accumulated monthly rainfall.
Females of P. capim had an average size at first sexual maturation (L50) of 24.91 mm (Fig. 3A), representing around 46% of the Lsof the largest female sampled. This length was 1.16 times greater than that of males, whose reached the size at first sexual maturation (L50) was 21.47 mm (Fig. 3B), representing approximately 36% of the Ls of the largest male sampled.
FIGURE 3| Average standard length of first sexual maturation (L50) of female (A) and male (B) of Pyrrhulina capim, sampled from March 2019 to March 2020 in the Guamá River basin, Eastern Amazon, State of Pará, Brazil.
The gonadosomatic index (GSI) did not vary across months for females (H = 10.188; df = 12; p = 0.599; Fig. 4A) and males (H = 14.908; df = 12; p = 0.246; Fig. 4B), indicating constant gonadal maturation activity throughout the year. Variations in the frequency of gonadal maturation stages in females showed the presence of immature individuals throughout the study period, with highest frequency (> 60%) in May, June, and July 2019, as well as January 2020. Mature females were absent in May and June 2019 and January 2020 but were more frequent in March and April 2019 and February 2020, coinciding with the greatest local precipitation rates. Resting females were not recorded in July 2019 and were frequent during periods of lower rainfall, except in to March 2019 and February 2020 (Fig. 5A).
FIGURE 4| Gonadosomatic Index variation (GSI) of females (A) and males (B) of Pyrrhulina capim sampled from March 2019 to March 2020 in the Guamá River basin, Eastern Amazon, State of Pará, Brazil. The dashed black line represents the accumulated monthly rainfall.
For males, the immature stage was recorded throughout the year, with greater frequencies in April, May, and June 2019. Maturating males were recorded for almost all months, except for June 2019, with higher frequencies in September and January. Finally, mature males were more frequent in March 2020 (Fig. 5B).
FIGURE 5| Gonadal maturation stage of female (A) and males (B) of Pyrrhulina capim sampled from March 2019 to March 2020 in the Guamá River basin, Eastern Amazon, State of Pará, Brazil. The dot indicates the average gonadosomatic index (GSI) for each month. The dashed black line represents the accumulated monthly rainfall.
The weight-length relationship did not differ between males and females (W = 19039; p = 0.143), demonstrating a similar growth pattern. Thus, the single weight-length relationship (Mt = 0.000009 x Ls3.12) showed positive allometric growth, with a proportional increase in weight exceeding that of length (Fig. S1).
The diameter of P. capim oocytes ranged from 0.05 to 0.70 mm, with a frequency distribution showing two modes: the first at approximately 0.20 mm (Fig. 6), called reserve oocytes and the second at approximately 0.50 mm (predominantly vitellogenic oocytes), indicating synchronous development in two groups. The smallest vitellogenic oocyte measured 0.367 mm in diameter. The estimated average fecundity of P. capim was 162 oocytes, ranging from 87 to 246 oocytes.
FIGURE 6| A. Variation in the oocyte diameter frequency of Pyrrhulina capim sampled from March 2019 to March 2020 in the Guamá River basin, Eastern Amazon, State of Pará, Brazil. The dashed red line indicates the minimum diameter of the vitellogenic oocytes. B. Mature ovary; C. Photomicrograph of mature ovary with oocytes in different stages of maturation: I, stage I oocyte; II, stage II oocyte; III, stage III oocyte; IV, stage IV oocyte.
Multiple Linear Regression (MLR), followed by the AIC selection criterion (Tab. S2), revealed that 13% of the variation in the GSI of females was positively influenced by wetted width (p = 0.001), sand (p = 0.001) , root (p = 0.043), organic matter (p = 0.002), and leaf bank percentages (p = 0.032), and negatively influenced by depth (p = 0.037) and silt percentage (p < 0.001) (Tab. 1). For males, environmental variables did not predict IGS variation.
TABLE 1 | Multiple Linear Regression Model showing the effects of the environmental variables in the Gonadosomatic Index variation (GSI) of female Pyrrhulina capim sampled from March 2019 to March 2020 in the Guamá River basin, Eastern Amazon, State of Pará, Brazil. ß = regression coefficient, SE = standard error, t = t statistic, p = p-value.
Response variable | Multiple regression | Environmental variables | ß | SE of ß | t | p |
Females GSI | R2 = 0.1335 | Wet width | 0.149 | 0.043 | 3.495 | 0.001 |
Depth | -0.029 | 0.014 | -2.097 | 0.037 | ||
F (7.212) = 5.821, p < 0.01 | % of sand | 0.056 | 0.016 | 3.473 | 0.001 | |
% of silt | -0.240 | 0.050 | -4.788 | <0.001 | ||
% of root | 0.037 | 0.018 | 2.039 | 0.043 | ||
AICc = 569.1 | % of organic matter | 0.103 | 0.032 | 3.213 | 0.002 | |
% of leaf bank | 0.029 | 0.013 | 2.161 | 0.032 |
Discussion
The pencil fish Pyrrhulina capim exhibited continuous reproductive activity throughout the studied period, characterized by group-synchronic ovarian development. Mature females displayed relatively small mature oocytes and low fecundity compared to other small-bodied species in Amazonian streams (López-Rodríguez et al., 2021; Oliveira et al., 2023). Gonadal maturation in females was not directly associated with rainfall regimes, as proposed by Kramer (1978), but was positively correlated with wider and shallower environments, which are indirectly influenced by rainfall. This activity was mainly dependent on microhabitat heterogeneity provided by substrate structure. The absence of a direct relationship with precipitation may also be associated with the fact that this variable was based on accumulated monthly precipitation rather than on precipitation in the days preceding the sampling of environmental conditions and specimens
The presence of larger males compared to females, combined with fin hypertrophy the dichromatism observed in some of individuals, reinforces the hypothesis that these traits are uses for attracting females (sexual display) and providing parental care, as evidenced in other species of this family (Krekorian, Dunham, 1972). Larger body size and secondary sexual characteristics are common in male teleost fish, often indicating greater vitality and resulting in advantages for their offspring (Helfman et al., 2009). However, not all sexually mature males of P. capim presented such characteristics, highlighting the need for further studies into the morphological variation among specimens.
The sex ratio of P. capim throughout the study followed the typical pattern of one male to one female did not differ from the pattern described by Vazzoler (1996), reinforcing the idea of a similar contribution of both sexes to offspring maintenance (Smith, 1972; Althoff et al., 2024). Despite the predominance of females in one of the driest months, this event does not appear to be associated with harem formation for initiating a new reproductive cycle, since reproductive activities occurred throughout the year. Instead, this predominance may reflect males’ preference for lateral pools, where they establish courtship and spawning territories. During low-rainfall periods, many of these lateral pools remain isolated and enriched with leaf litter, reducing the proportion of males in the main channel. Conversely, male migration to lateral pools during the rainy season alters the species composition of the main channels (Espírito-Santo, Zuanon, 2017). In the case, we believe that males of P. capim take advantage of these periods to access these areas and stands until the next rainy season.
The average length at first maturation, a reproductive tactic strongly related to growth and environmental conditions (Vazzoler, 1996), revealed that females of P. capim reached sexual maturity at greater lengths than males, reinforcing the pattern observed in other Lebiasinidae species, such as Nannostomus trifasciatus Steindachner, 1876 and Nannostomus marginatus (Eigenmann, 1909) (Althoff et al., 2024). For P. capim, the length at first sexual maturation for both sexes represented less than 50% of their maximum standard length, classifying the species as an early-maturing fish. This strategy, typical of small species like Deuterodon janeiroensis (Eigenmann, 1908) (Mazzoni et al., 2005), Diapoma alburnus (Hensel, 1870) (Fagundes et al., 2020) and Helogenes marmoratus Günther, 1863 (López-Rodríguez et al., 2021), may improve reproductive fitness in dynamics environments.
Females’ larges size at first maturation compared to males may be linked to the greater energy demand of oocyte production to sperm production (Wootton, 1992). This occurs mainly because oocytes are relatively larger cells compared to sperm (Wootton, Smith, 2014), and have a dense cytoplasm (Wootton, 1990), requiring a high amount of energy for development. Additionally, the “Gill-Oxygen Limitation Theory (GOLT)” hypothesis (Pauly, 2010; Pauly, Cheung, 2017; Pauly, 2019), may explain why males, despite their smaller size, meet the energy demands of sperm production due to lower oxygen requirements per unit of body mass (Wootton, 1992; Castro, 2021).
Variations in the mean length at first maturation may also reflect changes in environmental conditions (Roff, 1992). In disturbed habitats, premature maturation is often observed as a compensatory mechanism to maintain population viability (Guyonnet et al., 2003; Wootton, Smith, 2014). Although the studied microbasin predominantly influence by human activities, this is the first record of size at first maturation for P. capim, which prevents conclusions about the potential early maturation due to environmental disturbance.
The weight-length relationship of fish is also influenced by environmental conditions, as well as sex developmental stage of the individual (Bolger, Connolly, 1989). The positive allometric growth herein observed for P. capim differs from the isometric growth recorded for Pyrrhulina semifasciata Steindachner, 1876 (Favero et al., 2009) and Lebiasina erythrinoides (Valenciennes, 1850) (Urbano-Bonilla et al., 2016). Growth variations result from species-specific energy allocation influenced by extrinsic factors (e.g., environmental conditions) or intrinsic factors (for example, reproductive activity) (Jobling, 2002; Froese, 2006; Rêgo et al., 2008). For example, during reproduction, gonadal maturation and the development of secondary characteristics require high energy investment (Wootton, 1990), often reducing energy available for somatic growth.
The release of mature oocytes by females is directly related to the dynamics of oocyte development, the frequency of these spawning throughout the reproductive period, and the number of reproductive periods during their lives (Vazzoler, 1996). In this sense, P. capim exhibited a group-synchronic ovarian development (Wallace, Selman, 1981; Lubzens et al., 2010), consistent with batch spawning. This pattern differed from the total spawning observed for P. semifasciata in Central Amazon stream (Favero et al., 2009) and Nannostomus trifasciatus in the Unini River basin, Central Amazon (Althoff et al., 2024). This variation in the type of spawning may be directly related to the environment condition like flood pulse dynamics. On the other hand, batch spawning, common among stream fishes (López-Rodríguez et al., 2021; Oliveira et al., 2023), may enhance eggs fertilization and greater suitability for that experience seasonal changes environments (Vazzoler, 1996).
Fecundity can vary according to female growth, body size, environmental conditions, and food availability (Vazzoler, 1996). The species P. capim presented an estimated average fecundity of 190 oocytes, lower smaller quantity than P. semifasciata (939 oocytes), which ranged from 26 to 57.4 mm Ls (Favero et al., 2009) and L. erythrinoides (399–929 oocytes) that ranged from 20 to 160 mm Ls (Urbano-Bonilla et al., 2016). Body size may be the main factor influencing variation in fecundity when compared to other species in the family, as the number of oocytes increases according to body size (Wootton, 1992).
For P. capim, the presence of low fecundity and the ability to release oocytes repeatedly throughout the year appears to be advantageous. Low fecundity may also be associated with the presence of parental care, as previously evidenced in other lebiasinids through the morphological aspects of their eggs (Cordeiro et al., 2022) and behavioral observations (Krekorian, Dunham, 1972), which contribute to the success of the offspring.
The relationship between gonadal maturation in P. capim and environmental variables indicated a higher frequency of mature females in wider and shallower channels with a higher percentage of sand, roots, organic matter, and leaf banks in the stream substrate. This channel morphology with substrate type composed by elements provided from riparian vegetation likely increases the probability of forming the main microhabitats used by the species, such as backwater areas or lateral pools (Vieira, Netto-Ferreira, 2019). The hydrological conditions in these microhabitats retain significant amounts of organic matter, such as roots and leaf banks, which provide nutrients to the aquatic ecosystem (Tank et al., 2010; Souza et al., 2014), spawning sites, and shelters for larval and juvenile development. These results demonstrate that the maintaining P. capim populations depends on the structure of riparian vegetation, described as a key factor responsible for the primary productivity of stream ecosystems and the survival of aquatic organisms (Esteves et al., 2021; Lima et al., 2022). In this context, the occurrence of the species can serve as an important indicator of a healthy interaction between stream ecosystems and riparian vegetation, reinforcing the idea that the presence of Lebiasinidae species may be an important indicator of biotic integrity of Amazonian streams (Prudente et al., 2017).
The positive relationship between gonadal maturation activity and the percentage of sand in the streambed can also be attributed to the hydrological conditions of the microhabitats used by P. capim. In the Amazon, streams under natural conditions predominantly have sandy beds (Kemenes, Forsberg, 2014; Jacob et al., 2021). This predominance is even more evident in streams that drain lowland areas or in stream sections with lower current speeds, which favor the maintenance of this substrate. In contrast, the negative relationship between reproductive activity and percentage of silt in the streambed reinforces the sensitivity of P. capim to changes in stream ecosystems. Alterations caused by changes in land cover and use, tend to increase the amount of fine sediment in stream beds, reducing microhabitats heterogeneity (Prudente et al., 2017; Cantanhêde, Montag, 2024). Hirschler et al. (2024) also highlight the potential negative influence of silt on fish reproduction in the upper Piedmont portion of the Roanoke River basin in North Carolina and Virginia (USA). Much of the fine sediment runoff (mainly silt) into aquatic environments results from environmental impacts such as agriculture (Whitney et al., 2020; Moratelli et al., 2023) and urbanization (Hogan et al., 2014; Malhotra et al., 2020).
The lack of a relationship between environmental variables and gonadal maturation activity in male P. capim may be related to the lower energy demand for sperm maturation compared to oocyte maturation (Wootton, 1990). This lower energy requirement could enable males to undergo gonadal maturation throughout the year.
This work is pioneering in describing aspects of the reproductive biology of Pyrrhulina capim, evidencing reproductive activity throughout the year. Although not directly related to the rainfall regime, as proposed by Kramer (1978), reproduction in this species still depends on specific environmental conditions, which become more pronounced in the rainy season, as in the case lateral pool formations. While P. capim exhibits characteristics typical of an opportunistic reproductive strategy, such as continuous reproduction and low fecundity, the species also presents intriguing nuances.
The presence of larger males may also be related to male parental care, a behavior documented in certain species of the Lebiasinidae family, such as Copella arnoldi (Krekorian, Dunham, 1972). In such cases, larger male body size may provide advantages for offspring protection and the performance of complex parental behaviors (Krekorian, Dunham, 1972). Moreover, the low fecundity observed in P. capim lends further support to this hypothesis, as species with reduced reproductive output often compensate by increasing parental investment to enhance offspring survival (Winemiller, 1992). This reproductive strategy, typically associated with equilibrium strategists, has also been reported in other members of the family. The presence of traits characteristic of both opportunistic and equilibrium strategies (e.g., parental care) suggests a more complex life-history pattern in P. capim, in which elements of multiple reproductive strategies may coexist.
Finally, this study provides essential baseline information for defining conservation and sustainable management strategies, such as determining the average size at first maturation, which helps in the development of species-specific management and conservation plans (Fontoura et al., 2009). Considering the importance of Pyrrhulina species in the aquarium hobby market (Weitzman, Weitzman, 2003), our findings may also support the development of technological packages for breeding these species in captivity.
Acknowledgments
This research was conducted with financial support from the Universidade Federal Rural da Amazônia (UFRA), through a grant from the ‘Programa Institucional de Iniciação Científica’, funded by the PROPED 07/2020 Notice for the PROIC 2020/2021 cycle. Additional funding was partially provided by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES – Finance Code 001 to NCLR, process 1809704). We would also like to thank the UFRA, the “Laboratório de Ecologia e Conservação da Amazônia”(LABECA UFRA/Capitão Poço), and the “Laboratório de Histologia e Embriologia Animal” (UFRA/Belém) for providing the supportive research environment and granting access to the infrastructure necessary for of this project. I would also like to thank the reviewers and the editorial team for their valuable contributions to this manuscript.
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Authors
Marcilene Lima-Lima1 , Nathalia C. López-Rodríguez2, Elane Guerreiro Giese3 and Bruno da Silveira Prudente4
[1] Programa de Pós-Graduação em Ecologia Aquática e Pesca da Universidade Federal do Pará, Av. Bernardo Saião, Guamá, 68625 150 Belém, PA, Brazil. (MLL) marcilenelima003@gmail.com (corresponding author).
[2] Laboratório de Ecologia e Conservação da Amazônia (LABECA), Universidade Federal Rural da Amazônia, campus Capitão Poço, Rua Professora Antônia Cunha de Oliveira, Vila Nova, 68650-000 Capitão Poço, PA, Brazil. (NCLR) nathalyalopez616@gmail.com.
[3] Instituto de Saúde e Produção Animal, Universidade Federal Rural da Amazônia, Av. Presidente Tancredo Neves, 2501, Montese, 66077-901, Belém, PA, Brazil. (EGG) elane.giese@ufra.edu.br.
[4] Instituto Socioambiental e dos Recursos Hídricos, Universidade Federal Rural da Amazônia, Av. Presidente Tancredo Neves, 2501, Montese, 66077-901, Belém, PA, Brazil. (BSP) brunoprudente8@gmail.com.
Authors’ Contribution 
Marcilene Lima-Lima: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Writing-original draft, Writing-review and editing.
Nathalia C. López-Rodríguez: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Resources, Supervision, Writing-original draft.
Elane Guerreiro Giese: Methodology, Resources, Supervision, Visualization, Writing-original draft.
Bruno da Silveira Prudente: Conceptualization, Data curation, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Writing-original draft, Writing-review and editing.
Ethical Statement
Specimens collection was authorized by the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) through the Sistema de Autorização e Informação em Biodiversidade (SISBIO, license 63603), and the Ethics Committee for Animal Use of the Universidade Federal Rural da Amazônia (UFRA, process 054/2018).
Competing Interests
The author declares no competing interests.
How to cite this article
Lima-Lima M, López-Rodríguez NC, Giese EG, Prudente BS. Investigating the life history of Pyrrhulina capim (Characiformes: Lebiasinidae) in eastern Amazonian streams. Neotrop Ichthyol. 2025; 23(2):e240124. https://doi.org/10.1590/1982-0224-2024-0124
Copyright
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
Distributed under
Creative Commons CC-BY 4.0
© 2025 The Authors.
Diversity and Distributions Published by SBI
Accepted April 27, 2025
Submitted November 21, 2024
Epub August 04, 2025