Early ontogenetic development of Cynodon gibbus (Characiformes: Cynodontidae) in the Amazon River basin

Ruineris Almada Cajado^1,2,3 , Diego Maia Zacardi^1,4, Fabíola K. Souza Silva^1,4, Lucas Silva Oliveira^1,5 and Tommaso Giarrizzo^3,6

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Abstract​

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Introduction​

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The snub-nosed payara are neotropical fish belonging to family Cynodontidae, subfamily Cynodontinae, and genus Cynodon Agassiz, 1829, with records of two species, Cynodon gibbus (Spix & Agassiz, 1829) and Cynodon septenarius Toledo-Piza, 2000, in the Amazon basin (Dagosta, de Pinna, 2019). Morphologically and morphometrically, adult Cynodon differ from those of the other two genera in the family Cynodontidae, Hydrolycus Müller & Troschel, 1844 and Rhaphiodon Agassiz, 1829, with all species being found in the Amazon basin.

Adult Cynodon are distinguished from those in other cofamilial genera by their medium size, with a total length of up to 30 cm, silver-gray coloration, smooth and cycloid scales, short and deep body, transparent adipose fin, dorsal fin located at the beginning of the anal fin, higher count of rays in the anal fin, closed mouth forming an angle greater than 80°, and a dark rounded spot behind the superior margin of the gill opening and another at the base of the caudal fin (Toledo-Piza, 2000; Ohara et al., 2017).

Cynodon gibbus is a piscivorous predator that uses its canines teeth to hold prey, but it also occasionally feeds on invertebrates (Taphorn, 1992). Consequently, it plays an important role in maintaining the trophic chainbalance (Mérona et al., 2001). These species inhabit surface waters in rivers, lakes, and flooded forests, and have a wide geographic distribution in the Amazon and Orinoco River systems (Toledo-Piza, 2000; Fricke et al., 2024). They are medium-distance (between 500 and 1,500 km) migratory fish with a periodic life history strategy and large-sized reproductive traits, without parental care (Arantes et al., 2018; Cajado et al., 2023a). This species is used in fisheries, for subsistence and for commercialization as well as for sport fishing, specifically in clearwater rivers, such as Tapajós, Xingu, and Teles Pires (Ohara et al., 2017; Silvano et al., 2020). The heads of large individuals are used by artisans due to their long and sharp canines (Silvano et al., 2020).

Despite its economic, recreational, and ecological importance, the ecological and reproductive aspects of C. gibbus have not been extensively studied. Additionally, there is no published record of the initial development of this species; however, this record will be essential for identifying spawning areas and periods, larval drift as well as breeding and nursery habitats. Thus, we characterize the larval stages of C. gibbus based on general morphology and meristic and morphometric traits. Moreover, we also examine changes in these characteristics during ontogenetic development. We anticipate that this study will enable researchers to accurately differentiate snub-nosed payara larvae from those of other sympatric species and enhance our understanding of the early ontogeny of neotropical freshwater ichthyofauna.

Material and methods

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Collection of the larvae. Cynodon gibbus larvae were collected from various locations in the Amazon basin. Larvae were collected monthly along the main channel of the Xingu River (03º14’00”S 52º05’35”W and 03º29’43”S 51º42’28”W) in the years 2021, 2022, and 2023, and in the years 2013, 2014, 2017, 2018, and 2023, at sampling stations located in the main channel of the Amazon River (02º43’79”S 54º16’93”W and 01º59’04”S 55º25’48”W) and in the year 2015 at Maica Lake (02º28’42”S 54º38’04”W) in the lower stretch of the Amazon River, State of Pará, Brazil. Furthermore, trimestral collections were conducted in 2010 and 2011 in the proximity of the Reserva de Desenvolvimento Sustentável Mamirauá (03º08’S 64º45’W and 02º36’S 67º13’W), in the main channels of the Solimões and Japurá Rivers, State of Amazonas, Brazil (Fig. 1). All specimens used in this study were collected during daytime (15:00–18:00 h) or nighttime (20:00–23:00 h; UTC-3) using a local boat at low speed, with horizontal trawl nets in the subsurface of the water column with a plankton net (300 μm) for 5 or 10 min. The only exception were individuals in the postflexion stage, which were captured in floating macrophyte stands using a seine net (1 mm mesh size) measuring 5 m × 1.5 m.

FIGURE 1| Map of the Eastern Amazon depicting the sampling sites for Cynodon gibbus larvae collected in the study.

Analysis of biological material. After capture, all larvae were euthanized with benzocaine (250 mg/L) or 4-Alil-2-Metoxifenol (0.00005 mL/L) (according to the CONCEA Euthanasia Practice Guideline, 2013) before they were fixed in 10% formalin buffered with calcium carbonate. In the laboratory, C. gibbus larvae were sorted, separated from plant material and plankton, and identified through regressive sequence analysis, which involved comparing the morphology of more developed individuals with that of smaller ones (Ahlstrom, Moser, 1976). Subsequently, the larvae were classified into developmental stages following the terminology proposed by Ahlstrom et al. (1976) and modified by Nakatani et al. (2001), which includes the yolk-sac, preflexion, flexion, and postflexion stages.

The larval description was based on observation of the main morphological events and the degree of initial development. Additionally, meristic, and morphometric characters were considered, and the individuals that best represented the species’ characteristics were photographed and illustrated. The larval specimens used in this study are stored in the Coleção de Referência de Ovos e Larvas de Peixes at the Laboratório de Ecologia do Ictioplâncton e Pesca em Águas Interiores (CROLP-LEIPAI) of Universidade Federal do Oeste do Pará (UFOPA) (https://specieslink.net/col/CROLP-LEIPAI/) under the following catalog numbers: LEIPAI 520, LEIPAI 521, LEIPAI 522, LEIPAI 523, and LEIPAI 524.

Data analyses. In the larval stages yolk-sac, preflexion, and flexion, body length was measured as the distance between the snout tip and the final section of the notochord (SN). In postflexion larvae, when the caudal fin is fully formed and the notochord is completely flexed, we measured the standard length (SL), which is defined as the distance from the snout tip to the posterior margin of the hypural bones (Ahlstrom et al., 1976). To standardize data analysis, we regarded SN and SL as synonymous and referred to them as SL.

For the analysis of morphometric relationships (Ahlstrom et al., 1976), SL, head length (HL), snout length (SnL), eye diameter (ED), head depth (HD), body depth (BD), snout-dorsal fin distance (SnD), snout-anal fin distance (SnA), snout-pectoral fin distance (SnP), and snout-pelvic fin distance (SnV) were measured using a binocular stereomicroscope (Leica S9i) coupled with an integrated digital camera for image capture and software analysis (Leica LAS EZ-Heerbrugg, Switzerland). Additionally, the body depth toward the anus (BDA) was measured. During the larval yolk-sac and preflexion stages, the distance from the snout to the initiation point of the finfold located posterior to the anus was regarded as SnA. The morphometry of SnL, HD, and ED was expressed as a percentage of HL, whereas the other variables were expressed as a percentage of SL (Nakatani et al., 2001). For meristic characterization, were counted whenever possible, the preanal, postanal, and total number of myomeres, as well as the number of unbranched and/or branched rays present in the anal (A), dorsal (D), pectoral (P), pelvic (V), and caudal (C) fins.

For the morphometric relationship analysis of the larvae (expressed as a percentage), the variables HD, SnL, and ED were related to HL, whereas BD, BDA, HL, SnA, SnD, SnP, and SnV were related to SL. Body relationships for BD (BD/SL), HL (HL/SL), and ED (ED/HL) were established using the criteria described by Leis, Trnski (1989) modified by Nakatani et al. (2001). The proportions of HD to BDA and BD were explored to elucidate the morphometric relationships throughout the development.

To evaluate body growth patterns, regression models were used wherein the morphometric variables (dependent variables), except BDA, were plotted against SL and HL (independent variables). These relationships were described by different growth models, which could be used to infer biological processes linked to early ontogeny (Kováč et al., 1999). The hypothesis of continuous isometric growth was tested using a simple linear regression model. Two alternative developmental hypotheses, listed as follows, were also tested: gradual allometric growth (quadratic regression) and discontinuous isometric growth (piecewise linear regression, characterized by breakpoints that highlight divergent growth rates). The most suitable model linking each morphometric variable to the body and head size were determined using F tests. In the absence of significance, growth was evaluated using the simplest model. A “p” value of <0.05 was considered significant. All statistical analyses were performed in the software R v. 4.1.1 using the package Segmented (Muggeo, 2008).

Results​

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Forty-eight larvae were studied at various stages development (two yolk-sacs, 35 preflexion, 10 flexion, and one postflexion) with a SL ranging from 5.73 to 21.57 mm. No phenotypic differences were observed among individuals collected from different rivers and environments (e.g., channel and lake).

Morphological and meristic characterization. Yolk-sac stage (Tab. 1; Fig. 2A). The standard length ranges from 5.73 to 5.81 mm (5.77±0.04 mm). The yolk-sac is elliptical, and the notochord is straight and visible owing to transparency. The body is elongated in a fusiform shape, and the snout is rounded. The mouth is semi-open in a subterminal position. The nostrils are simple, the otolith is visible, and the opercula partially cover the gill cavity. The eyes are spherical, brown, and poorly pigmented. Moreover, the terminal part of the intestine slightly overtakes the middle region of the body. The color pattern consists of two small punctate pigments in the fontanelle, dendritic at the end of the yolk, in the rectum, in the region of origin of the anal fin, and in a dashed shape at the upper and lower ends of the caudal peduncle. The embryonic membrana (finfold) encompasses the entire dorsal and ventral region of the body, being interrupted only by the anus, with no clear differentiation between dorsal, caudal, and anal fins. The pectoral fin button is visible but small. The myomeres are, clearly visible, and 51–52 in number (25 preanal and 26–27 postanal).

TABLE 1 | Variables analyzed (mm), minimum values (Min), maximum values (Max), mean (Mean), standard deviation (SD), and morphometric relationships (%) for Cynodon gibbus larvae. SL = standard length, HL = head length, SnL = snout length, ED = eye diameter, HD = head depth, BD = body depth, SnD = snout–dorsal fin distance, SnA = snout–anal fin distance, SnP = snout–pectoral fin distance, SnV = snout–pelvic fin distance, BDA = body depth toward the anus, AF = absent fin, NV = rays not visible or absents, n = number of individuals.

Variables (mm)	Yolk-sac (n = 2)		Preflexion (n = 35)		Flexion (n = 10)		Postflexion (n = 1)
	Min–Max	Mean±SD	Min–Max	Mean±SD	Min–Max	Mean±SD	Min–Max	Mean±SD
SL	5.73–5.81	5.77±0.04	5.94–8.64	6.99±0.62	8.62–16.33	12.25±2.56	21.57	–
HL	0.90–0.90	0.90±0.00	1.12–1.61	1.27±0.11	1.60–3.50	2.45±0.60	4.98	–
SnL	0.19–0.25	0.22±0.03	0.26–0.51	0.35±0.06	0.41–0.88	0.58±0.13	1.25	–
ED	0.19–0.20	0.20±0.00	0.18–0.32	0.22±0.03	0.27–0.61	0.41±0.10	1.01	–
HD	0.67–068	0.67±0.01	0.64–1.02	0.79±0.08	0.95–2.12	1.40±0.38	2.75	–
BD	0.76–0.87	0.81±0.06	0.55–1.16	0.71±0.12	0.85–2.16	1.43±0.43	3.15	–
BDA	0.36–0.40	0.38±0.02	0.32–0.58	0.40±0.05	0.54–1.40	0.93±0.32	2.61	–
SnD	AF	AF	AF	AF	4.64–8.68	6.70±1.27	11.29	–
SnA	3.43–3.45	3.44±0.01	3.75–5.35	4.24±0.38	5.29–8.91	7.07±1.25	11.53	–
SnP	AF	AF	1.10–1.70	1.31±0.12	1.67–3.38	2.45±0.56	4.98	–
SnV	AF	AF	AF	AF	AF	AF	9.75	–
Morphometric proportions (%)
ED/HL	21.65–22.66	22.15±0.50	14.45–20.21	17.66±1.44	14.79–19.30	16.83±1.29	20.34	–
HD/HL	74.22–75.67	74.94±0.73	51.68–71.73	62.34±4.20	50.52–64.04	57.23±4.32	55.20	–
HL/SL	15.43–15.65	15.54±0.11	15.68–20.09	18.23±0.84	18.35–21.44	19.82±1.03	23.08	–
SnL/HL	20.87–28.13	24.50±3.63	18.92–36.89	27.82±3.85	17.74–32.46	24.29±4.65	25.14	–
BD/SL	13.02–15.20	14.11±1.09	8.50–13.40	10.16±1.21	8.70–14.19	11.57±1.65	14.58	–
BDA/SL	6.15–7.02	6.59±0.44	4.84–6.70	5.71±0.50	5.49–9.21	7.47±1.21	12.10	–
SnD/SL	AF	AF	AF	AF	52.36–60.15	54.93±2.16	52.34	–
SnA/SL	59.45–59.83	59.64±0.19	58.07–62.47	60.58±1.16	54.55–62.35	58.16±2.27	53.46	–
SnP/SL	AF	AF	16.34–20.92	18.73±0.96	18.68–20.92	19.92±0.75	23.08	–
SnV/SL	AF	AF	AF	AF	AF	AF	45.19	–
Myomeres
Preanal	25	25 (n = 2)	25–26	25 (n = 15)	25–26	26 (n = 6)	26	–
Postanal	26–27	26 (n = 1)	26–27	26 (n = 16)	26–27	27 (n = 5)	27	–
Total	51–52	51 (n = 1)	51–53	52 (n = 11)	52–53	53 (n = 4)	53	–
Number of rays
Dorsal	NV	NV	NV	NV	8–10	8–10	ii,11	–
Anal	NV	NV	NV	NV	36	36	ii,78	–
Pectoral	NV	NV	NV	NV	NV	NV	14	–
Pelvic	AF	AF	AF	AF	AF	AF	NV	–
Caudal	NV	NV	NV	NV	15–18	15–18	18	–

FIGURE 2| Larval development of Cynodon gibbus. A. Yolk-sac (5.81 mm SL); B. Preflexion (6.44 mm SL); C. Early flexion (9.70 mm SL); D. Late flexion (15.22 mm SL); and E. Postflexion (21.57 mm SL). Scale bars = 1 mm.

Preflexion stage (Tab. 1; Fig. 2B). Individuals have an SL ranging from 5.94 to 8.64 mm (6.99±0.62 mm). The notochord is straight and visible owing to transparency. Some specimens with an SL of 6.78 mm had yolk remnants. The body is elongated in a fusiform shape; the snout is pointed; and the mouth is subterminal, large, oblique, and has numerous conical teeth externally. The nostrils are simple, and the eyes are spherical, fully pigmented, and black in preserved individuals. The swim bladder is visible, inflated, and oval shaped. The intestine is vertically striated, and elongated, and the anal opening reaches the midline of the body. The pigmentation is similar to that of the previous stage. Dendritic melanophores are observed in the apical region of the swim bladder, in the embryonic membrane just below the stomach, but are scarce at the origin of the anal fin. The finfold still surrounds the body dorsoventrally, being interrupted only by the anus. The pectoral fin bud is small and surrounded by a membrane, not reaching the swim bladder. Total number of myomeres ranges from 51 to 53 (25–26 preanal and 26–27 postanal).

Flexion stage(Tab. 1; Figs. 2C–D). The SL ranges from 8.62 to 16.33 mm (12.25±2.56 mm). The final SN is flexed by the emergence of the hypural bones. Morphologically, the body, snout, mouth, nostrils, eyes, and position of the anus show no change in relation to the previous stage. The swim bladder assumes a triangular shape. The gill apparatus is covered by the operculum, a feature not observed in earlier stages. The pigmentation is analogous to that of the preflexion stage, but pigments appear on the hypural plate and on the caudal rays. At this stage, the delineation of the unpaired fins is observed. Individuals with 15.22 mm SL have the first dorsal and anal fin rays. Anal fin is located just after the beginning of the dorsal fin base, making them overlap. The finfold is still visible in the ventral region, from the stomach to the anus and in the region post dorsal fin, origin of the adipose fin, and caudal peduncle. At the end of this stage, the caudal fin shows well-developed rays, and its shape is changed from truncated to forked. The pectoral fin still lacks rays. The total number of myomeres ranges from 52 to 53 (25–26 preanal and 26–27 postanal).

Postflexion stage(Tab. 1; Fig. 2E). The SL of the analyzed individual is 21.57 mm. The notochord and swim bladder are visible owing to transparency. The pigmentation pattern is similar to that of the previous stage but more intense, particularly in the caudal peduncle and in the caudal rays. Some pigments weakly radiate from the base of the anal fin into the rays. All fins, except for the pelvic one, are in the final developmental phase, including ray segmentation. Remnants of the finfold can be observed in the ventral region anterior to the anus and dorsally situated between the dorsal and anal fins, and extending toward the caudal peduncle. The adipose fin is outlined, and the pelvic fin is only visible as a bud. Most of the rays of the pectoral fin are completely formed (i,13). The anal fin is long and has numerous rays (ii,78), beginning slightly posterior to the midpoint of the body, and perpendicular to the dorsal fin, which has ii,11 rays. The caudal fin has 18 rays (9 in each lobe, superior and inferior). Notably, all unpaired fins are segmented and branched. The total number of myomeres is 53 (26 preanal and 27 postanal).

Morphometric relationships. Throughout development, the body varies from very long to long (8.5 to 15.20% of SL), and the eyes are small (14.45 to 22.66% of HL); the head is initially small but becomes moderate in the preflexion stage (15.68 to 20.09% of SL) (Tab. 1). The proportions of most morphometric variables increased with development, except for SnD/SL, SnL/HL, and SnA/SL, which decreased with development (Tab. 1).

Body growth relationships. The depth of the head and the length of the snout tend to increase in proportion to HL and exhibited continuous linear growth (linear regression). The remaining growth relationships are better explained by the quadratic model and exhibit positive allometry, except for SnA/SL, which showed negative allometric growth, decreasing its distance to the snout during development (Tab. 2; Figs. 3A–G). The variables SnD/SL and SnV/SL were not tested due to the small number of individuals in which these variables were measured, making the application of regression models unfeasible.

TABLE 2 | Values of linear (L), quadratic (Q), and piecewise (S) regression analyses of morphometric variables in relation to head length (HL) and standard length (SL) of Cynodon gibbus larvae. R² = coefficient of determination. BM = best model. Values in bold represent a significant difference (p < 0.05). HD/HL = relationship between head depth and head length, BD/SL = relationship between body depth and standard length, HL/SL = relationship between head length and standard length, SnL/HL = relationship between snout length and head length, ED/HL = relationship between eye diameter and head length, SnA/SL = relationship between snout–anal fin distance and standard length, SnP/SL = relationship between snout–pectoral fin distance and standard length, n = number of individuals.

Variables	R2			Test F			BM	n
	L	Q	S	Q/L	S/Q	S/L
SnL/HL	0.86	0.86	0.87	3.20	2.23	2.77	L	48
ED/HL	0.95	0.97	0.98	34.01	3.26	19.67	Q	48
HD/HL	0.98	0.98	0.98	0.55	5.07	2.84	L	48
BD/SL	0.94	0.96	0.96	16.51	2.57	9.89	Q	48
HL/SL	0.99	0.99	0.99	23.19	1.38	12.41	Q	48
SnA/SL	1.00	1.00	1.00	28.93	3.72	17.38	Q	48
SnP/SL	0.99	0.99	0.99	25.40	3.16	15.04	Q	46

FIGURE 3| Body ratios (mm) between head length and snout length (A); head length and eye diameter (B); head length and head depth (C); standard length and body depth (D); standard length and head length (E); standard length and distance from snout to pectoral fin (F); and standard length and distance from snout to anal fin (G) during the early development of Cynodon gibbus. Ysl = yolk-sac, Pre = preflexion, Fle = flexion, Pos = postflexion.

Discussion​

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This study describes, for the first time, the morphological, meristic, and morphometric characteristics of C. gibbus larvae, and is the first one to describe Cynodontidae larvae, except for the larval description of Rhaphiodon vulpinus Spix & Agassiz, 1829 (Nakatani et al., 2001; Sousa, Severi, 2002) in several biotopes of the Pantanal, Mato Grosso, and the Paraná basin, Brazil. Throughout early ontogeny, C. gibbus larvae exhibit characteristics typical of fish that have minimal individual investment per offspring. Initially, they are poorly developed, lacking fins, with only the pectoral fin bud and a finfold that is absorbed during development. These characteristics are similar to the larvae of fish that do not provide parental care (Garcia et al., 2016; Ticiani et al., 2022).

The larvae exhibit the general characteristics of Cynodontidae, such as an elongated body, small eyes, and an oblique, wide mouth equipped with numerous conical teeth externally (Nakatani et al., 2001; Sousa, Severi, 2002; RAC, pers. obs.). Having a wide mouth equipped with numerous conical teeth externally is considered a synapomorphy of Cynodontidae (Toledo-Pizza, 2000), distinguishing fish larvae of this family from those of any other species of Characiformes. The oval swim bladder in preflexion and triangular in flexion and postflexion, the number of preanal and postanal myomeres, and the coloration pattern with pigments around the rectum and caudal peduncle are specific features of C. gibbus (Fig. 4), which distinguish them from other Cynodontidae species (Nakatani et al., 2001; Sousa, Severi, 2002). The larvae exhibit predominantly allometric growth patterns, such that the body structures tend to increase or decrease more rapidly than SL and HL.

FIGURE 4| Diagnoses of morphological characteristics of Cynodon gibbus larvae. Scale bar = 1 mm.

Taxonomy of fish larvae involves the combined use of meristic, morphological, and morphometric techniques, common for identifying these organisms throughout their life stages (Garcia et al., 2016; van der Sleen, Albert, 2017). However, the characters used tend to differ from those used for adult individuals due to the absence of certain structures and intense changes that occur during the early ontogeny of fish (Marancik et al., 2020; Tietler et al., 2021; Oliveira et al., 2022).

The larvae of C. gibbus can be distinguished from those of species of Hydrolycus in that they have overlapping dorsal and anal fins, visible at the end of the preflexion stage, the tip of the pectoral fin does not reach the anterior margin of the swim bladder, and by having 25–26 preanal myomeres and 26–27 postanal myomeres, whereas the larvae of Hydrolycus armatus (Jardine, 1841) and Hydrolycus scomberoides (Cuvier, 1819)lack overlapping fins, because the dorsal fin positioned ahead of the anal fin, the distal limit of the pectoral fin reaching the swim bladder, and having 30–32 and 28–29 preanal myomeres and 19–21 and 21–23 postanal myomeres, respectively (RAC, pers. obs.). Additionally,having a total of 51–53 myomeres, the number of preanal myomeres, pigmentation on the rectum, and caudal peduncle distinguish C. gibbus from R. vulpinus, which has over 60 total myomeres, over 37 preanal myomeres, and no pigmentation in the rectum region and caudal peduncle (Nakatani et al., 2001; Sousa, Severi, 2002). Finally, an oval–triangular-shaped swim bladder distinguishes C. gibbus from species of both genera, as they have an elliptical swim bladder (Fig. 5). The color pattern characterized by pigmentation in the upper and lower extremities of the caudal peduncle as well as the presence of pigments at the base of the caudal fin in more developed individuals, can be used to distinguish C. gibbus larvae from C. septenarius, which lacks this pigmentation at the base of the caudal rays (Toledo-Piza, 2000).

FIGURE 5| Principal morphological differences among larvae of Cynodontidae. A. Cynodon gibbus; B. Hydrolycus spp.; C. Rhaphiodon vulpinus. Larvae of R. vulpinus adapted from Sousa, Severi (2002). Scale bars = 1 mm.

The C. gibbus larvae at the yolk-sac stage are rudimentary, having lightly pigmented eyes, a toothless mouth, and a non-functional anus, characteristics similar to those of R. vulpinus (Sousa, Severi, 2002). Our findings indicate that the acquisition of eye functionality (pigmentation) in C. gibbus coincides with the partial absorption of the yolk, emergence of teeth, and development of both oral and anal openings in the preflexion stage. At this stage, we also observed the inflated swim bladder, which, as noted by Santos et al. (2016) and Blecha et al. (2019), plays a crucial role in the maneuverability, stability, and vertical balance of the larvae in the water column. The simultaneous development of these organs, at the interface between endogenous and exogenous feeding, is essential because it enables the larvae to detect, capture, and consume food, thus contributing to survival in the early stages, which are considered the most critical in the life history of fish (Godinho et al., 2003; Santos et al., 2023). Similarly, presence of the pectoral fin bud at the early larval stages seems to be an important feature for larval survival. This is because the pectoral fin, during these stages, functions as an enhancer of gas and/or ionic exchange in fluids close to the body, aiding in ventilation and cutaneous respiration, as the gills are not yet capable of meeting the larvae’s oxygen metabolic demands (Green et al., 2012; Hale, 2014; Zimmer et al., 2020).

Growth models related to morphological changes indicate variations in ecological and functional aspects during the early ontogenetic stages of C. gibbus. Rapid changes in external appearance, dimensions, and the differential growth of structures or body parts, known as allometry, are common features during the early ontogeny of teleost fishes in continental waters (Andrade et al., 2016; Silva et al., 2022; Ticiani et al., 2022; Xu et al., 2023). In highly mobile and voracious swimmers, such as C. gibbus, these alterations are associated with the timing of crucial events in the early life history, such as changes in water column position, feeding habits, and swimming ability (Santos et al., 2017; Oliveira et al., 2022; Shin et al., 2022). Therefore, the rate of development of certain structures is adjusted based on the ecological needs of the larvae as they grow (Bialetzki et al., 2008; Martínez-Montaño et al., 2016; Kupren et al., 2023).

The positive allometry of the eyes reveals a trend of more rapid growth of this organ relative to the head during larval development in C. gibbus, which aligns with the observed pattern in the initial ontogeny of other Characiformes, which typically exhibit discontinuous allometry or isometry (piecewise growth) (Santos et al., 2020; Cajado et al., 2021; Silva et al., 2022; Souza et al., 2023). The rapid growth of the eyes, along with the pigmented retina, indicates a priority in the development of this organ and, consequently, the need for sharper vision from the early larval stages of C. gibbus. As with other fish, the ability to see plays a significant role in the survival of C. gibbus larvae, as it allows locating and selecting favorable habitats, as well as detecting prey and predators (Yahaya et al., 2011; Miranda et al., 2020; Nowosad et al., 2021). High visual resolution promotes selective feeding, potentially leading to variations in diet composition throughout the various stages (Santin et al., 2004; Makrakis et al., 2005).

The wide mouth equipped with multiple teeth and a pointed snout indicates that the larvae of C. gibbus are efficient predators, as observed in the larvae of other morphologically similar Characiformes, such as Brycon spp. and Salminus spp. (Oliveira et al., 2012; Araújo et al., 2020; Ribeiro, Portella, 2020; Lima et al., 2021). Additionally, the striate in the intestine suggests a high capacity for expansion of this organ, a characteristic associated with the consumption of relatively large and nutritious prey, such as the larvae of other fish (Makrakis et al., 2005; Pepin, 2023). However, in preliminary analyses, most of the larvae had empty stomachs, and when there was food, it consisted of small zooplanktonic organisms such as cladocerans and copepods (RAC, pers. obs.). These findings differ from what was observed in the larvae of H. armatus, H. scomberoides, and R. vulpinus, which primarily feed on larvae of other Characiformes (RAC, pers. obs.). This discrepancy can be attributed to prey availability, interspecific competition, and niche partitioning (Picapedra et al., 2018; Silva, Bialetzki, 2019; Kume et al., 2021). Further studies investigating the ontogeny of feeding habits can provide a clearer understanding of the relationship between morphology and food capture in these fish.

The allometric growth of BD (BD/SL) and HL (HL/SL) reflects body remodeling and an enhancement of locomotor and cognitive abilities, as well as trophic level expansion during the early ontogeny of C. gibbus, as observed in the larvae of other freshwater fish(Silva et al., 2022; Xu et al., 2023). The rapid growth rate of BD/SL reveals a tendency for the transformation from an elongated body shape to a more heightened body as the larvae develop. The pattern observed in BD/SL indicates the prioritized development of organs related to the digestive tract, musculature, and pectoral girdle (Oldani, 2005; Kupren et al., 2015; Marinho, 2023). The absence of significant changes in snout proportions (SnL/HL) and HD (HD/HL), as indicated by linear growth, suggests minimal variations in feeding habits throughout the stages of development C. gibbus (Abelha et al., 2001; Makrakis et al., 2005).

The positive allometric changes of HL/SL suggests the accelerated development of organs associated with vital functions, such as the respiratory system (e.g., gills and operculum) and cranial structures (e.g., teeth, nostrils, and mouth) (Santos et al., 2020; Franz et al., 2021; Silva et al., 2022). Although a similar change is expected for HD/HL, the morphology of the larval cephalic region, with an elongated snout and head tending to increase from small to moderate, likely demands a much more accelerated growth of HL/SL than in HD/HL. An example of this rapid development is the growth of the operculum, which becomes prominent at the end of the flexion stage, completely covering the gills. The complete covering of the gills by the operculum in the flexion stage of C. gibbus differs from what is observed in most larvae of Characiformes, in which this occurs in the preflexion stage (Bialetzki et al., 2008; Oliveira et al., 2022; Cajado et al., 2023b). However, it resembles what is observed in other cynodontids, such as R. vulpinus and Hydrolycus (Sousa, Severi, 2002; RAC, pers. obs.). At this stage, there may be a transition from cutaneous respiration to gill respiration in C. gibbus, as observed by Rombough (2002) and Zimmer et al. (2020) for Danio rerio (Hamilton, 1822) larvae, which tend to rely fully on their gills to obtain oxygen during the flexion stage (21 days post-fertilization). Similarly, the accelerated increase in HL is likely related to the need for space to accommodate the expansion of the mouth, as well as the emergence and growth of teeth during early ontogeny. This is crucial as C. gibbus is a piscivorous species, and the development of these structures should maximize predation and, consequently, survival rates.

Emergence and segmentation of rays in C. gibbus leads to changes in swimming capacity and positioning of larvae in the water column, as observed in other fish species with planktonic larvae (Santos et al., 2020, 2023). This is enabled by the allometry of SnP/SL and SnA/SL, which, along with the increase in the number of rays, suggests a shift from planktonic larval status to a nektonic behavior, allowing the exploration of new habitats and water column strata as development progresses. The negative allometry observed in SnA/SL in C. gibbus appears to be associated with changes in the origin of the fin as the larvae grow. Negative allometry also occurs in the increased curvature of the posterior section of the intestine in postflexion.

In less developed C. gibbus individuals (yolk-sac larva, preflexion, and early flexion stages), the anal fin (considering the distance from the snout to the origin of the embryonic fin after the anus) appears after the midbody point (62.70–58.10% of SL in yolk-sac larva, preflexion, and early flexion stages). In more developed individuals, it appears closer to the midbody point (54.55–53.46% of SL late flexion and postflexion). The approximation of the anal fin to the midbody point is similar to what is observed in adults; however, in adult individuals, the anal fin originates slightly ahead of the dorsal fin (Toledo-Piza, 2000). Despite the substantial changes that the C. gibbus larvae will undergo until reaching adulthood, such as increased head height and changes in mouth and fin positions, the number of branched rays in the anal fin (78) of the largest individual analyzed resembles that observed in adults (65 to 80 branched rays), distinguishing post-flexion larvae of this species from that of any other in the family and potentially similar Characiformes, such as Galeocharax spp. (Toledo-Piza, 2000; Giovannetti et al., 2017).

In conclusion, the integrative approach, which considers a combination of characteristics such as fin position, swim bladder shape, pectoral fin range, pigmentation patterns, and the number of myomeres (including pre- and postanal myomeres), enables the identification of early stages of C. gibbus larvae. This contribution is valuable for future taxonomic studies, specifically those related to ichthyoplanktonic communities captured in their natural environment. The growth patterns of various body parts reveal fundamental morphological changes essential for the survival of C. gibbus larvae during early development. These studies are crucial for identifying spawning sites, nurseries, and larval drift.

Acknowledgments​

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This study is part of the thesis of the first author (RAC) at the Postgraduate Program on Aquatic Ecology and Fishing, Universidade Federal do Pará. Special thanks to Zaqueu Santos for creating the illustrations of the species, and to our colleagues from the Universidade Federal do Oeste do Pará, represented by the Laboratório de Ecologia do Ictioplâncton e Pesca em Águas Interiores, for their valuable assistance in the collection, sorting, and identification of the biological material used in this study. RAC is funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). TG is funded by National Council for Scientific and Technological Development (CNPq #308528/2022–0). Part of this study was also financed by Norte Energia S.A. (PMI-2022), Brasília, DF, in the federal environmental licensing process for UHE Belo Monte (02001.011114/2020–52), and by the Ministério da Ciência, Tecnologia, Inovações e Comunicações (MCTIC) and the Instituto de Desenvolvimento Sustentável Mamirauá (IDSM).

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Authors

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Ruineris Almada Cajado^1,2,3 , Diego Maia Zacardi^1,4, Fabíola K. Souza Silva^1,4, Lucas Silva Oliveira^1,5 and Tommaso Giarrizzo^3,6

^[1]    Laboratório de Ecologia do Ictioplâncton e Pesca em Águas Interiores, Universidade Federal do Oeste do Pará, Rua Vera Paz, s/n, Salé, 68040-255 Santarém, PA, Brazil. (RAC) ruineris.cajado@gmail.com (corresponding author), (DMZ) dmzacardi@hotmail.com, (FKSS) fabiola.katrine@gmail.com, (LSO) lucasmdcpa@gmail.com.

^[2]    Universidade do Estado do Amapá, Av. Presidente Vargas, 650, Central, 68900-070 Macapá, AP, Brazil.

^[3]    Núcleo de Ecologia Aquática e Pesca da Amazônia, Programa de Pós-Graduação em Ecologia Aquática e Pesca, Universidade Federal do Pará, Av. Perimetral, 2651, 66040-830 Belém, PA, Brazil. (TG) tgiarrizzo@gmail.com.

^[4]    Programa de Pós-Graduação em Biodiversidade, Instituto de Ciências e Tecnologia das Águas, Universidade Federal do Oeste do Pará, Rua Vera Paz, s/n, Salé, 68040-255 Santarém, PA, Brazil.

^[5]    Programa de Pós-Graduação em Ecologia, Instituto de Ciências Biológicas-ICB, Universidade Federal do Pará, Av. Perimetral, 2651, 66040-830 Belém, PA, Brazil.

^[6]    Instituto de Ciências do Mar (LABOMAR), Universidade Federal do Ceará (UFC), Avenida da Abolição, 3207, Meireles, 60165-081 Fortaleza, CE, Brazil.

Authors’ Contribution

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Ruineris Almada Cajado: Conceptualization, Formal analysis, Investigation, Methodology, Software, Writing-original draft.

Diego Maia Zacardi: Data curation, Project administration, Resources, Writing-original draft, Writing-review and editing.

Fabíola K. Souza Silva: Formal analysis, Investigation, Methodology, Visualization, Writing-original draft.

Lucas Silva Oliveira: Investigation, Methodology, Visualization, Writing-original draft.

Tommaso Giarrizzo: Resources, Supervison, Validation, Visualization, Writing-review and editing.

Ethical Statement​

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The collection of biological was realized under authorization granted by the Sistema de Autorização e Informação em Biodiversidade (SISBIO) of the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBIO) and Ministério do Meio Ambiente (MMA) of Brazil, authorizations numbers 75271–1/2020, 7233 and 23741–1, issued based on the Normative Instruction number 154/2007 and followed the euthanasia protocols in accordance with the norms of the Conselho Nacional de Controle e Experimentação Animal(CONCEA, 2013).

Competing Interests

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The author declares no competing interests.

How to cite this article

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Cajado RA, Zacardi DM, Silva FKS, Oliveira LS, Giarrizzo T. Early ontogenetic development of Cynodon gibbus (Characiformes: Cynodontidae) in the Amazon River basin. Neotrop Ichthyol. 2024; 22(3):e240012. https://doi.org/10.1590/1982-0224-2024-0012

Copyright​

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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.

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© 2024 The Authors.

Diversity and Distributions Published by SBI

Accepted July 23, 2024 by Andrea Bialetzki

Submitted February 10, 2024

Epub October 07, 2024