Ontogeny and point-of-no-return of Amazon banded cichlid Heros severus larvae

Abstract

This study describes the embryonic and larval development of the ornamental fish Heros severus, and the effects of delaying its initial feeding, providing insights for its captive breeding. Experiment 1 describes the embryonic and larval until hatching. The Experiment 2 determined the point-of-no-return (PNR) and evaluated the effect of delaying the first feeding on the development and survival of H. severus larvae. This experiment consisted of 10 treatments represented by the day of first feeding (delays of 1 to 10 days to first feeding), and two controls (positive: larvae continuously fed; negative: not-fed larvae. The cleavage occurred at 55 minutes post- fertilization and hatching at 53 hours post-fertilization at a water temperature of 28±0.5°C. The newly hatched larvae showed average total length of 4.18±0.18mm and remained attached to the substrate until mouth opening, which was observed at 125 hpf, when they filled the gas bladder and initiated swimming movements. The longer was the time for first feeding, the lower was larval weight and length. However, one day of feed deprivation did not affect larval development. The estimated point-of-no-return for H. severus larvae were 6 and 8 days for PNR50 and PNR100, respectively.

Key words
larviculture; fasting time; PNR; embryonic development; ornamental fish

INTRODUCTION

In 2021, the global trade in ornamental fish sector, including fish, aquarium accessories, tanks, fish feed, medicines, plants, and services, was estimated to be around US$ 30 billion (Anikuttan et al. 2023). This trade encompasses the exchange of over 2 billion units of live ornamental fish (Hui et al. 2020, Yue 2019), emphasizing the role of developing countries as the largest producers and suppliers of ornamental fish worldwide. In this context, Singapore stands out as the leader in exports, contributing approximately 20% of the global total (Anikuttan et al. 2023).

Among the commercially traded species of ornamental fish, the cichlids present remarkable diversity, with approximately 1,727 species, making it the third most traded fish family in the Amazon Basin (Rodrigues et al. 2009, Queiroz et al. 2013, Beltrão et al. 2019, Tribuzy-Neto et al. 2021). Among the Amazonian cichlids, the severum cichlid, Heros severus Heckel, 1840, holds great potential for trade due to its beautiful color and adaptability to aquaculture (Abe et al. 2016). Prices for a single specimen measuring around 5 cm in total length can exceed US$ 20 (Aquarium 2021). Despite its international value, there is a scarcity of studies on its early development, which is essential for establishing efficient captive breeding protocols.

Understanding fish ontogeny is crucial, as it provides insights on the morphology of important structures and the chronology of their differentiation during the initial development of the species. This information is fundamental for aquaculture, offering knowledge about the appropriate management practices for larviculture (Santos et al. 2022b). It also allows for the observation of critical points such as fertilization, hatching, and mouth opening, aiming at optimizing growth and survival (Valbuena-Villarreal et al. 2012). In addition, this type of study can provide information about the development of the digestive and immune systems (Zapata 2006) and the timeframe during which the larvae fully absorb their endogenous energy reserves. In this way, by knowing the development of structures throughout development, rearing techniques can be adapted to meet the abilities and limitations of larvae at each stage of their development, thus increasing survival and growth rates (Portella et al. 2014).

One of the main causes of mortality during fish larviculture is their nutritional condition. When larvae undergo prolonged fasting or feed restriction, morphophysiological alterations occur, leading to adverse effects on their development (Kolkovski et al. 2009, Kanazawa 2003). The point-of-no-return (PNR) is defined when the effects of feed deprivation become irreversible, and animals die even when the food becomes available (Xu et al. 2017, Chen et al. 2018, Garcia et al. 2020). Therefore, understanding the PNR during fish larviculture is useful to identify the maximum time that larvae can remain in starvation after yolk consumption and recover when food is offered. This strategy can be helpful in cases of unpredictable situations during intensive rearing. However, there is a scarcity of PNR studies for cichlids (Paes 2008) and it is inexistent for H. severus. Thus, this study was conducted aiming at describing the embryonic and larval development of H. severus, as well as the effects of delaying its initial feeding, providing insights for its captive breeding.

MATERIALS AND METHODS

All the following procedures were approved by the Ethical Committee of Embrapa Tabuleiros Costeiros (N. 038/2022). Larvae and eggs of H. severus were collected from natural spawns of captive breeders and were maintained at temperature of 28.1±0.5°C, pH of 7.2±0.2, dissolved oxygen of 4.2±0.3 mg/L, ammonia of 0.00 ± 0.00 mg/L and nitrite of 0.00 ± 0.00 mg/L.

First experiment – ontogenetic development

After the spawn of 5 pairs, egg samples (n=4) were collected every ten minutes for the first two hours, starting the collection once the male had completed the fertilization, and registering the number of minutes post fertilization (mpf). Subsequently, samples were collected every hour until hatching, recorded in hours post fertilization (hpf). Afterwards, the samples were taken every 12 hours, registering the hours-degree (hd) until the complete larval development (adapted from Radael et al. 2013). The description of embryonic development was carried out according to Woynarovich & Horváth (1983) and Nakatani et al. (2001) dividing the embryo development into the following phases: newly fertilized egg, blastula, morula, gastrula and larvae at the time of hatching. After hatching, the larval development was evaluated in samples of larvae (n=4) collected every 12 hours and analyzed according to Blaxter (1988) and Gomes et al. (2003). Morphological characteristics observed in larval phase, such as changes in pigmentation and time of mouth and anus opening, were recorded.

The observation and recording of embryo and larval development were carried out using a BEL phototonics optical microscope coupled to a camera and a computer software (BEL capture) to analyze the images (photomicrography equipment; with precision of 0.1 mm).

The biometric measurements were determined as follows:

- Egg: egg diameter (mm; D1 = larger diameter and D2 = smaller diameter), perivitelline space (mm), yolk diameter (mm), and egg volume ​​​(​​µL​)​​ ​(​​1​)​​​​.

- Larvae: total length (mm), yolk volume ​​​(​​µL​)​​ ​(​​1​)​​​​, and eye diameter (mm).

(¹) Egg volume and yolk volume ​​​(​​µL​)​​ = π / 6 ∙ D1 ∙ D2

Second experiment – point-of-no-return (PNR)

This experiment, which lasted 15 days and utilized larvae 5 days after hatching, was carried out in a completely randomized design with ten treatments (T1-T10 corresponding to 1 to 10 days of feed deprivation before first feeding), a positive control (PC, larvae continuously fed), and a negative control (not-fed larvae), in triplicates.

A total of 180 larvae were distributed into 36 polyethylene tanks containing one liter of water (5 larvae/liter) in a static system without aeration. The photoperiod was maintained at 12 hours of light and 12 hours of darkness (12L:12D). Newly hatched Artemia nauplii were offered in the fed treatments four times a day at the concentration of 250 nauplii/larvae (Abe et al. 2016). The residues accumulated on the bottom of the tanks were siphoned and 50% of the water was renewed daily. The water used for renewal had the following parameters: a temperature of 28.1±0.5°C, pH of 7.2±0.2, dissolved oxygen of 4.2±0.3 mg/L, ammonia of 0.01±0.00 mg/L, and nitrite of 0.01±0.00 mg/L.

At the end of the experiment, the following zootechnical parameters were recorded or estimated as follows:

• Total length (mm);

• Weight (g);

• Survival (S; %) = (final number of larvae/initial number of larvae) × 100;

• Specific Growth Rate (SGR; %/d) = 100 {[Ln (final body weight) − Ln (initial body weight)]/experimental days} × 100;

• Relative Condition Factor (Kn) = ​​\frac{Ow}{Ew}, where Ow = observed weight and Ew = estimated weight (Le Cren 1951); a Kn value was calculated for each larvae and a mean and standard deviation were calculated for each treatment;

Initially, for the calculation of Kn, the weight-length relationship was estimated to calculate the estimated weight using the formula: W = ​a . Lb​, where the constants (a and b) were estimated by linear regression from transforming the equation into: Log W = Log a + b Log L. Where W = weight; L = length; a = intercept; b = angular coefficient (Portella et al. 2000, Santos et al. 2022a).

• $$\text{Uniformity (U)}=\frac{{\sum }_{p=1}^3xf}{{\sum }_{f=1}^{3}xp}\times 100$$, where xf = number of larvae weighing ±20% of the mean weight, xp = total number of survivors, p and f = each repetition (Furuya et al. 1998).

The moments when 50% (PNR50) and 100% (PNR100) of the mortality were observed according to Blaxter & Hempel (1963).

Statistical analysis

Data were tested for normality and homoscedasticity using the Shapiro-Wilk and Bartlett tests, respectively, followed by analysis of variance (ANOVA) and Tukey test to compare the means of the treatments (Zar 2010). The points-of-no-return (PNR50 and PNR100) were estimated using Generalized Linear Models (GLM). For all tests, a significance level of 0.05 was adopted. All statistical analyzes were carried out using the R software, version 4.0.5 (R Development Core Team 2021).

RESULTS

First experiment – ontogenetic development

At an average temperature of 28.1±0.5°C, the formation of the blastodisc and syncytial layer occurred 30 minutes after fertilization or 14 hd (Fig. 1a, Table I). The eggs showed a perivitelline space of 0.33±0.12 mm, with a volume of 2.95±0.67 µL. The eggs exhibited two main characteristics: adhesiveness and oval shape (Fig. 1a).

Figure 1
Development phases of the egg: (a) egg with oval shape; (b) Blastodisc cleavage (4 blastomeres); (c) Blastodisc with 32 blastomeres; (d) Morula phase; (e) Gastrulation; 20% epiboly; (f) Gastrulation, 30% epiboly; (g) Gastrula, 80% of epiboly; (h) Formation of the cephalic region (CE) and pair of otoliths; (i) Morphogenesis and organogenesis; tail development (MOR), and somites hyperplasia.

Table I
Embryonic development of Heros severus eggs.

Phases	Sub-phase	mpf* or hpf**	hd***	Figure
Blastula	1 cell	30*	14	1a
	4 cells	35*	15	1b
	32 cells	43*	20	1c
Morula	64 cells	55*	24	1d
Gastrula	Start	1**	28	1e
		2**	56	1f
	End	13**	364	1g
	Cephalic region	29**	812	1h
	Fin development and somites	52**	1456	1i

• *mpf = minutes post-fertilization; **hpf = hours post-fertilization; ***hd = hours-degree.

The hatching occurred after 53 hpf (Fig. 2a), with larvae showing 4.18±0.18 mm of total length, yolk sac volume of 2.39±0.56 µL and adhesive glands on the top of their head. The larvae became attached to the substrate and were cared by their parents. At 72 hpf, the larvae showed initial eye pigmentation, which had a diameter of 1.91±0.04 mm. At 98 hpf, the larvae showed fully pigmented eyes and the pectoral fin started to differentiate (Fig. 2c, Table II). After 125 hpf, the larvae opened their mouth (Fig. 2d, Table II) and anus, filled the gas bladder and initiate active swimming movements. After 147hpf, the development of the cardiac atrium and ventricle development was observed (Fig. 2e, Table II) and at 172 hpf, it was possible to observe the presence of gills (Fig. 2f, Table II). Finally, at 196 hpf, approximately 8 days after hatching, the digestive system presented organs already developed, which were observed by transparence (Fig. 3).

Figure 2
Development phases of Heros severus larvae: (a) Hatching, 53 hpf (yolk-sac larvae); (b) Initial eye pigmentation, 72 hpf, AG – Adhesive glands; PO – Pair of otoliths; (c) Eye completely pigmented, mouth formation, irregular heart tube, and development of the pectoral fin, 98 hpf; (d) Mouth and anus opening and swim bladder filling 125 hpf; (e) Development of the heart – AV-formation of the atrium and ventricle, 147 hpf; EX – Excretion of bile through the anus ; (f) Formation of gill filaments – GB, 172 hpf.

Figure 3
Observation of the digestive system, presence of the rays in the caudal fin and pigmentation of Heros severus larvae (196 hpf).

Table II
Larval development of Heros Severus.

Phases	Hpf*	**	Figure
Hatching	53	1484	4a
Initial eye pigmentation, appearance of a pair of otoliths	72	2016	4b
Final eye pigmentation and formation of pectoral fin	98	2744	4c
Mouth opening, gas bladder filling, and active swimming	125	3500	4d
Appearance of the atrium and ventricle	147	4116	4e
Formation of the gills	172	4816	4f
Development of the digestive system and presence of rays in the caudal fin (?)	196	5488	5

• *hpf = hours post-fertilization; **hd = hours-degree.

Second experiment – point-of-no-return (PNR)

In experiment 2, the longer were the fasting days, the lower were the larvae length and weight (Table III). Nonetheless, feeding deprivation of one day did not affect the larval growth compared to the positive control. Larvae of the treatments T8, T9, T10 and negative control died after eight days of feed deprivation, even after feeding.

Table III
Mean values (± standard deviation) of the zootechnical parameters of Heros severus larvae submitted to different periods of feed deprivation.

Treatments	TL (mm)	W (g)	SGR (%)	U (%)	Kn
PC	10.94±0.63a	0.0200±0.0039a	12.55±1.31a	93.33±9.42	1.06±0.13a
T1	10.61±0.83ab	0.0187±0.0027a	11.97±1.10ab	100±0.00	1.06±0.15a
T2	9.83±0.75bc	0.0148±0.0021b	10.57±1.08b	83.33±23.57	0.95±0.14a
T3	8.96±0.93cd	0.0117±0.0021c	8.96±1.26c	100±0.00	0.85±0.14ab
T4	8.90±0.50cd	0.0114±0.0015c	8.89±0.94c	91.66±11.78	0.81±0.11b
T5	8.66±0.75de	0.0104±0.0023cd	8.15±1.76c	100±0.00	0.79±0.09b
T6	8.12±0.38de	0.0087±0.0008cd	7.07±0.73c	100±0.00	0.77±0.06bc
T7	7.95±0.76e	0.0077±0.0016d	6.13±1.46c	88.88±15.71	0.65±0.12c

• TL, Total length; W, weight; SGR, specific growth rate; U, uniformity for weight; Kn, relative condition factor; PC, positive control; T1 to T7, treatments with 1 to 7 days of feed deprivation; different letters in the columns mean statistical difference using the Tukey’s test (p<0.05).

A delay of up to 4 days for the first feeding did not affect the final survival of the larvae (Fig. 4). However, feeding delays longer than five days (T5 to T10) reduced the survival with total mortality at 8 days of feed deprivation (p< 0.05) (Fig.4). The points-of-no-return with 50% and 100% of mortality (PNR50 and PNR100) were determined at 6 and 8 days, respectively (Fig. 5).

Figure 4
Mean values and standard deviation of the survival rates of Heros severus larvae submitted to different periods of feed deprivation. Different letters indicate statistical difference by Tukey’s test (p < 0.05).

Figure 5
Survival rates at the end of the 15 experimental days and point-of-no-return (PNR50 and PNR100) of Heros severus larvae. The arrow indicates the PNR100.

DISCUSSION

The Amazonian ornamental fish Heros severus is a non-migratory species, and their eggs exhibit specific characteristics, including adhesiveness (Rizzo et al. 2002). The adhesiveness is attributed to the presence of glycoconjugates on the egg’s surface, typically secreted by mucus-producing cells found in the oocytes (Nelson et al. 2019). The oocytes become sticky in the presence of water, enabling them to adhere to the substrate. Newly hatched H. severus larvae exhibited a pair of highly developed adhesive glands in the frontal region of the head. These adhesive glands play a crucial role in larval attachment to the surface throughout the larval development (Santos et al. 2002). Groppelli et al. (2003) also reported the presence of adhesive glands in other ornamental cichlids, Pterophyllum scalare.

The eggs of H. severus have a small perivitelline space (0.33 mm) rather than the larger perivitelline space (0.8 mm) seen in cyprinids. This difference is related to the need for egg protection against external physical impacts (Wang et al. 2021, Sohn & Kim 2021) and the presence or absence of parental care (Goodwin et al. 1998). A small perivitelline space (0.1-0.5 mm) is frequent among cichlids. A similar perivitelline space (0.29 mm) was observed in the cichlid discus, Symphysodon aequifasciatus (Swain et al. 2020).

The gills developed later in H. severus larvae, suggesting that these larvae likely utilized their skin for gas exchange before the complete development of a functional gill epithelium. Additionally, the gut of fish larvae is typically not fully functional before yolk sac consumption (Wilson & Castro 2010).

During the larval period, the yolk provides the necessary energy and nutrients until mouth opening and beginning of exogenous feed (Shields 2001, Yanagitsuru et al. 2021). However, after mouth opening, coupled with a decline of the endogenous energy supply, the consequences of feed restriction become harmful to fish development (Wang et al. 2017, Gong et al. 2017). In their natural environment, fish larvae often experience periods of feed deprivation due to factors such as climatic fluctuations leading to feed scarcity, such as floods or droughts (Leggett & Deblois 1994). During feed deprivation, fish larvae exhibited an increase in locomotor activity to enhance their chances of finding feed. However, in cases of prolonged restriction, a decrease in physiological activity leading to mortality (Oliveira et al. 2020, Kojima et al. 2015, Holt 2011, Gadomski & Petersen 1988). This was observed in H. severus larvae, with mortality reaching 50% and 100% after 6 (PNR 50) and 8 (PNR 100) days of feed deprivation, respectively. In this study, larvae from the positive control and T1 achieved the highest values of length and weight compared to the other treatments. Larvae submitted to one day of feed deprivation (T1) showed complete growth compensation, likely due to hyperphagia and improved feed conversion, allowing for the recovery of larval growth (Ali et al. 2003). Conversely, the other treatments, with extended periods of feed deprivation, hindered normal larval growth, probably because energy reserves were utilized for survival rather than for increasing body size (Nebo et al. 2013). The lower weight of H. severus larvae after 2 days of feed deprivation suggests delays in muscle formation compared to larvae fed normally. This corroborates the findings reported by Nebo et al. (2013), who subjected larvae of juvenile tilapia (Oreochromis niloticus) to feed deprivation and observed that juveniles deprived for 5 days showed lower weight and reduced expression of genes responsible for the proliferation of muscle cells (myogenin and myostatin). Larvae of pacu (Piaractus mesopotamicus) subjected to feed deprivation also exhibited decreased weight related to a reduction in the muscle fiber diameter and a smaller number of hyperplasic fibers compared to continuously fed larvae (Leitão et al. 2011, Kojima et al. 2015).

In the present study, it was observed that the points of no return (PNR50 and PNR100) of 6 and 8 days, respectively, for H. severus larvae were similar to with those estimated by Kojima (2015) for pacu larvae (6 days and 8 days for PNR50 and PNR100, respectively, at 29 °C). After 5 days of feed deprivation, pacu reduced their feeding rate by 50% compared to non-fasted animals, indicating that feed deprivation can affect feeding behavior (Kojima et al. 2015). Similarly, altricial goldfish larvae (Carassius auratus), a cyprinid, also presented PNR50 and a PNR100 on the 6 day and 8 day of feed deprivation, respectively, at the temperature of 26 °C (Motta 2018). The point-of-no-return represents the stage in which the larva has already undergone several deteriorating processes, including alterations in the enzymatic activity, utterly leading to feeding inability (Dabrowski 1982). However, the concentration of proteins and lipids, as well as histopathological and enzymatic changes, were not determined in this study. Therefore, future research should aim at providing a comprehensive understanding of energy utilization during feed deprivation for H. severus larvae. The effects of delayed feeding on hematopoietic organs, intestine, pancreas, and enzyme activity must also be evaluated for this species.

CONCLUSIONS

In conclusion, the observation of the ontogeny of H. severus allowed for the determination of appropriate feeding management for larvae to ensure high survival and normal growth. Continuous feeding or one-day delay in initial feeding is recommended for H. severus larval rearing. The possibility to delay the first feeding is a useful information in the case of unforeseen circumstances during H. severus larviculture.

ACKNOWLEDGMENTS

The authors confirm that the data supporting the findings of this study are available within the article. The authors would like to thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the financial support to RYF (304533/2019-0) and MCP (307389/2021-9).

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Publication Dates

• Publication in this collection
  21 Feb 2025
• Date of issue
  2025

History

• Received
  02 Oct 2024
• Accepted
  28 Oct 2024