Early development in the mouth-brooding cichlid fish Satanoperca pappaterra (Perciformes: Cichlidae)
Desarrollo temprano en el pez cíclido Satanoperca pappaterra (Perciformes: Cichlidae)
Taise Miranda Lopes1*, Fernando Garcia de Oliveira1, Andréa Bialetzki1,2* & Angelo Antonio Agostinho1,2
Abstract
The Neotropical region exhibits the largest diversity of fish worldwide; however, little is known about the early development of fish species from this region. Therefore, to contribute to this knowledge, this study aimed to morphologically describe the early stages of development (eggs, larvae and juveniles) of S. pappaterra using morphometric and meristic traits, and to assess changes in growth rates throughout larval and juvenile development by analyzing the relationships between various morphometric traits using analytical regression models. Both juvenile and adult individuals with mouth-brooded offspring were collected along the basins of the Cuiabá and Manso Rivers in the state of Mato Grosso, Brazil between March 2000 and March 2004. After the adults were identified, the offspring were classified according to its stage (embryonic, larval or juvenile period), and various morphometric and meristic variables were individually measured (when possible). The eggs of this species are yellow in color, oval shaped, show dendritic pigmentation within their yolk, have small to moderately sized perivitelline spaces and lack a mucous membrane and oil droplets. The horizontal and vertical diameters of the sample yolks ranged from 1.43mm to 2.70mm and 1.05mm to 1.68mm, respectively. The standard length of the larval period varied from 4.30mm to 7.16mm, and the standard length of the juvenile period varied from 10.29mm to 24.57mm. Larvae exhibit yolk sacs with internal dendritic pigmentation and dark punctate pigmentation in the dorsal and ventral body regions, whereas irregular transverse spots along the flanks are observed during the juvenile period. Adhesive organs are only present during the yolk-sac stage and at the beginning of the flexion stage. The mouth is terminal during all stages of development. The myomere number varied from 22 to 29 (9 to 16 pre-anal and 10 to 16 post-anal), and the maximal numbers of fin rays and spines were as follows: dorsal, XVI+10; anal, IV+8; pectoral, 16; and pelvic, I+8. Growth analyses identified periods of important change in larval morphology (i.e., metamorphosis), particularly during the flexion and post-flexion stages and in juveniles. Therefore, the morphological development of S. pappaterra is consistent with the ecological requirements of this species, which primarily occurs in structured lentic environments with aquatic macrophytes. Rev. Biol. Trop. 63 (1): 139-153. Epub 2015 March 01.
Resumen ]]>
La región Neotropical exhibe la mayor diversidad de peces en todo el mundo. Sin embargo, poco se sabe sobre el desarrollo temprano de las especies de peces de esta región. Para contribuir a este conocimiento, este estudio tuvo como objetivo describir morfológicamente las primeras etapas de desarrollo (huevos, larvas y juveniles) de S. ]]>
usando rasgos morfométricos y merísticos. Además de evaluar los cambios en las tasas de crecimiento en el desarrollo larval y juvenil, mediante el análisis de las relaciones entre los diferentes rasgos morfométricos utilizando modelos de regresión analíticos. Tanto los individuos juveniles y adultos con crías de incubación bucal se recogieron a lo largo de las cuencas de los ríos Cuiabá y Manso en el estado de Mato Grosso, Brasil, entre marzo 2000 y marzo 2004. Después de ]]>
S. pappaterra es consistente con las ]]>
Palabras clave: ontogenia, huevos, larvas, peces, incubación bucal, Río Paraguay.
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The greatest difficulty inherent to the study of freshwater ichthyoplankton is properly identifying fish eggs and larvae in their natural environments. This difficulty stems largely from the significant morphological similarities between different taxonomic groups during early stages of development (Bialetzki, Sanches, Baumgartner, & Nakatani, 1998) and because species spawn in the same areas at the same times of the year (Nakatani et al., 2001). Hence, the taxonomic characterization of early fish ]]>
Cichlidae is the second largest of the 160 characterized families within the order Perciformes, and it is composed of nearly 1 300 species worldwide and approximately 291 in ]]>
Cichlasoma nigrofasciatum (Gunther, 1868) (Martinez & Murillo, 1987); Cichlasoma gadovii (Regan, 1905) (Cabrera, ]]>
Cichlasoma dimerus (Heckel, 1840) (Meijide & Guerrero, 2000); Astronotus ocellatus (Agassiz, 1831) (Nakatani et al., 2001; Paes, Makino, Vasquez, Fernandes, & Nakaghi, 2011); Archocentrus myrnae (Loiselle, 1997) (Puigcerver, 2007); Amphilophus rostratus (Gill, 1877) (Molina, 2008); Apistogramma cacatuoides (Hoedeman, 1951) (Alves, Rojas, & Romagnosa, 2009);
Hypsophrys nicaraguensis (Günther, 1864) (Molina, 2011); and Pterophyllum scalare (Schultze, 1823) (Korzelecka-Orkisz et al., 2012). In contrast, early development in Neotropical mouth-brooders has not yet been described. Differences in the dynamics of larval and post-larval development between these two groups have been noted not only in terms of external morphology but also in terms of the maturation of several vital organs (Fishelson, 1995). According to Fishelson, the offspring ]]>
Satanoperca pappaterra (Heckel, 1840), which is commonly known as the Pantanal eartheater and locally known as ‘cará’ or ‘acará,’ is a mouth-brooding endemic species from the Amazon Basin (Rio Guaporé) and upper Paraguay River (Kullander, 2003). Within the Amazon Basin, this species ]]>
Satanoperca acuticeps (Heckel, 1840), Satanoperca daemon (Heckel, 1840), Satanoperca jurupari (Heckel, 1840) and Satanoperca lilith (Kullander & Ferreira, 1988), and none of these species has been characterized with respect to their early stages of development. Considering the high degree of morphological similarity within this genus as well as the ]]>
S. pappaterra using morphometric and meristic traits and (ii) assess changes in the growth rates throughout larval and juvenile development by analyzing the relationships between various morphometric traits using analytical ]]>
Materials and Methods
Study site: The samples used in this study were collected between March 2000 and March 2004 at different locations along the Cuiabá and Manso river basins ]]>
Fig. 1), both of which are part of the Paraguay River hydrological basin.
Sampling: Both juveniles and mouth-brooding adults carrying eggs and/or larvae were collected using seining nets (20m length, 1cm mesh size). After capture, the adults released their offspring, which were immediately collected and placed into polyethylene bottles and fixed with 4% formaldehyde buffered with calcium carbonate.
Characterization of developmental stages: The collected individuals were separated into embryonic (early cleavage, early embryo and tail-free stages), larval (yolk-sac, flexion and post-flexion stages) and juvenile periods in accordance with the classifications proposed by Ahlstrom & Ball (1954) and modified by Nakatani et al. (2001). Each period was described based on the degree of development and occurrence of major morphological events, with representative individuals illustrated using a camera lucida. Individuals used in this research have been deposited in the Ichthyological Collection of the Center for Research in Limnology, Ichthyology and Aquaculture (Nupélia) at the State University of Maringá (Universidade Estadual de Maringá - UEM), Paraná, Brazil (NUP 16905 to NUP 16908 and NUP 13676).
For the morphological characterization of embryonic development, the following morphometric variables were measured (in mm) using a stereoscope equipped with an ocular micrometer: egg diameter (EgD), yolk diameter (YD) and perivitelline space (PS), with the latter categorized as narrow, moderate, large or very large based on its share of the total egg volume (Nakatani et al., 2001). For both YD and PS, the horizontal diameter was defined as the major axis corresponding to the distance between the animal and vegetal poles, and the vertical diameter was defined as the axis with the smallest diameter. For the larvae and juveniles, the following parameters were also measured (in mm) (according to Ahlstrom, Butler, & Sumida, 1976; Nakatani et al., 2001): standard length (SL), snout length (SnL), eye diameter (EyD), head height (HH), head length (HL) body height (BH), pre-pectoral (SPcF), pre-pelvic (SPlF), pre-dorsal (SDF) and pre-anal (SAF) fin distances. Meristic characterizations were performed by counting, when possible, the number of pre- and post-anal myomeres and number of rays in the pectoral (Pc), pelvic (Pl), dorsal (D) and anal (A) fins. The body ratios for EyD, BH and HL were determined using the categories proposed by Leis & Trnski (1989).
Growth models: To identify potential ontogenic variations during the larval and juvenile periods, the morphometric variables (dependent variables) were plotted against a standard and the HL (explanatory variables), and their relationships were analyzed using various regression models (Kováč, Copp, & Francis, 1999). First, we tested the hypothesis that body ratio development is continuously isometric using a simple linear regression model. In addition, we also tested two alternative hypotheses: gradual allometric growth by using a quadratic regression analysis and discontinuous isometric growth by using a piecewise linear regression analysis, which is characterized by breakpoints reflecting divergent growth rates. The optimal models for each morphometric variable relative to body and head size were determined using F tests (Sokal & Rohlf, 1981). The significance level for the analyses was p<0.05.
Results
In total, 60 eggs (20 in the early cleavage, 20 in the early embryo and 20 in the tail-free stage), 88 larvae (20 in the yolk-sac, 48 in the flexion and 20 in the post-flexion stage) and 21 juveniles were analyzed. Each period is described below and illustrated in figure 2 and figure 3. Results related to morphometry, meristic counts and body ratios for the different periods are shown (Table 1, Table 2 and Table 3), and the results from the regression analyses of larval and juvenile growth are shown in table 4.
Embryonic period: In general, the eggs were yellow (apart from the internal dendritic pigmentation throughout the yolk) and oval shaped, had narrow PSs and lacked oil droplets and mucosal outer membranes (Fig. 2a and Fig. 2c). Embryos in the final stage of development were not found among the analyzed samples.
Early cleavage stage: The eggs had a mean horizontal diameter of 2.05mm and vertical diameter of 1.63mm (Table 1). The PSs ranged from narrow to moderate, with mean diameters (relative to the egg) of 6.89% horizontally and 4.86% vertically. In most cases, the egg membranes were oval shaped, which was similar to the shape of the yolk (Fig. 2a).
Early embryo stage: The eggs had a mean horizontal diameter of 2.01mm and vertical diameter of 1.51mm (Table 1). The PSs ranged from narrow to moderate, with mean diameters (relative to the egg) of 9.04% horizontally and 5.54% vertically. Within the yolk, formation of the embryonic axis was evident, and it extended from one pole to the other in the form of a continuous strip that bifurcated around the blastopore (Fig. 2b). ]]>
Tail-free stage: The eggs had a mean horizontal diameter of 2.07mm and vertical diameter of 1.53mm (Table 1). The PSs ranged from narrow to moderate, with mean diameters of 11.23% horizontally and 9.15% vertically. At this stage, it is possible to observe a distinction between the body and head of the larva along the embryonic axis. The unpigmented forming eyes, notochord and punctate pigmentation within the posterior caudal region can also ]]>
Fig. 2c). In the final phase of this stage, the caudal region begins to separate from the yolk, although it remains attached.
Larval period: None of the larvae examined were in the pre-flexion stage; other stages are described below. ]]>
Yolk-sac stage: In this stage, the SL ranged from 2.00mm to 4.15mm (Fig. 3a) (Table 2). Although it is possible to observe slight flexion of the notochord, the hypural bones have not yet formed. The yolk sac features internal dendritic pigmentation and is relatively large compared with the size of the larva. The eyes are elliptical and partially pigmented, and they do not ]]>
Flexion stage: The analyzed larvae were between 4.30mm and 5.75mm (Fig. 3b and Fig. 3c) (Table 2). The ]]>
Post-flexion stage: The SL of the samples ranged from 6.34mm to 10.25mm (Fig. 3d) (
Table 2). By this stage, the digestive system has formed (visible by transparency), and an anal opening is located medially to the body axis. The eyes are elliptical and pigmented, and the operculum is defined. Nasal apertures are simple. The finfold is fully absorbed, and the dorsal and anal fins have defined shapes, with the onset of ray segmentation beginning at approximately 7.0mm SL. All rays of the caudal fin are segmented. The dorsal fin exhibits between XIII to XV spines and 10 to 12 rays, whereas the anal fin has III spines and 6 to 8 rays. From 6.67mm SL onward, the pectoral fin exhibits between 10 and 14 fully segmented ]]>
Juvenile period: The SL of the samples ranged from 10.29mm to 24.57mm (Fig. 3e) (Table 2). The eyes ]]>
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Body ratios: Three variables were analyzed over the course of ontogenic development and standardized relative to the HL. Head height (HH) decreased during development and ranged from 138.03% to 79.49%. Snout length (SnL) decreased between the yolk-sac and flexion stages (20.74% and 13.95%, respectively) and increased during the two remaining stages (18.40% and 26.91%, respectively). Eye diameter (EyD) increased during each larval stage, ranging from moderate to large (25.00% to 76.47% during yolk-sac; ]]>
Table 3).
Six other variables were analyzed relative to SL. Head length (HL) showed an increase in relation to SL, ranging from small during the yolk-sac stage to large during the ]]>
Table 3). ]]>
Growth models: With respect to the body growth analyses, SnL and HH showed discontinuous isometric growth (piecewise linear regression) relative to HL (from 0.50mm and 1.87mm, respectively) during development (Table 4); in particular, we observed a change in growth rate during the post-flexion stage (Appendix). Based on the slopes of the data, these variables showed higher growth rates ]]>
Table 4). Eye diameter (EyD) showed continuous isometric growth (linear regression), meaning that EyD showed constant growth throughout the course of development.
For the variables related to SL, the results indicated that HL, BH and the SPcF, SP1F, and SAF distances ]]>
Table 4 and Appendix). With the exception of BH, which showed increased growth during the post-flexion stage, the other variables decreased relative to growth rate at the beginning of either the flexion (for HL and SP1F and SAF distances) or juvenile (for SP1F distance) stages. The SDF distance showed quadratic development, meaning that it showed variable growth that initially increased and ]]>
Table 4 and Appendix).
Discussion
The identification ]]>
S. pappaterra, are indicative of species with long larval development times (Vazzoler, ]]>
C. nigrofasciatum, Martinez, & Murillo, 1987); H. nicaraguensis (Molina, 2011); A. rostratus (Molina, 2008); and Amphilophus alfari (Meek, 1907) (Molina, 2010) produce eggs with similar dimensions to those of
S. pappaterra, with the eggs varying from 2.00mm to 2.25mm along the horizontal axis and from 1.55mm to 1.72mm along the vertical axis; C. dimerus (Meijide & Guerrero, 2000) is an exception and produces smaller eggs (1.65mm±0.05mm horizontal diameter and 1.25mm±0.05mm vertical diameter). With respect to mouth-brooders, the eggs of Oreochromis mossambicus (Peter, 1852) are significantly larger than ]]>
S. pappaterra, with a horizontal diameter of 3.04mm±0.20mm and vertical diameter of 2.19mm±0.16mm (Holden & Bruton, 1992). Therefore, the dimensions of S. pappaterra eggs are more similar to those of previously characterized substrate ]]>
Within the family Cichlidae, internal pigmentation of the yolk during the embryonic period appears to be a reliable taxonomic characteristic of this group. For example, ]]>
A. ocellatus, which was described by Nakatani et al. (2001) and Paes et al. (2011), shows strong pigmentation within the yolk sac from the embryonic period until full absorption, which is similar to what was observed for S. pappaterra; the same pigmentation occurs during the embryonic stages of the species C. ]]>
(Cabrera et al. 1988)), C. dimerus (Meijide & Guerrero, 2000) and Oreochromis niloticus (Linnaeus 1758) (Nakatani et al., 2001; Fujimura & Okada, 2007), although the pigmentation is less intense.
Characterizing the shape and ]]>
A. ocellatus (Nakatani et al., 2001; Paes et al., 2011), O. niloticus (Nakatani et al., 2001; Fujimura & Okada, 2007), C. nigroasciatum (Martinez & Murillo, 1987), H. nicaraguensis (Molina, 2011) and S. pappaterra, the presence of dendritic pigments in the upper region of the head at the onset of the larval period appears to be a common trait. With respect to body pigmentation, S. pappaterra larvae differ from other species by the presence of pigmented regions in the dorsal and ventral regions. At the ]]>
S. pappaterra has 5 or 6 transverse spots, C. nigrofasciatum has 8 or 9 transverse spots (Martinez & Murillo, 1987) and O. niloticus has 7 transverse spots (Nakatani et al., 2001; Fujimura & Okada, 2007). In contrast, H. nicaraguensis ]]>
A. ocellatus shows intense pigmentation throughout its entire body as well as between the rays of its fins (Nakatani et al., 2001; Paes et al., 2011).
From an ecological perspective, pigmentation patterns may play protective roles against predation. ]]>
A. ocellatus, Machado-Allison (1987) observed that the larvae develop a highly disruptive pigmentation pattern in natural environments, which allows a perfect camouflage against predators when the larvae are hidden among ]]>
Hoplias malabaricus, Hoplosternum littorale and Prochilodus lineatus), which has been described by Nakatani, Baumgartner and Cavicchioli (1997) and Nakatani, Bialetzki, Baumgartner, Sanches and Makrakis (2004).
With respect to ]]>
S. pappaterra. This phenomenon occurs extremely early and is unusual at this stage of development compared with other species. In addition, of the analyzed larvae, specimens in the pre-flexion stage were not found. Therefore, we believe that the pre-flexion stage in S. pappaterra may be short or even absent, which could be useful for identifying larval individuals.
The presence of adhesive glands is also an important characteristic for species identification. For example, C. dimerus (Meijide ]]>
A. ocellatus (Nakatani et al., 2001; Paes et al., 2011) and H. nicaraguensis (Molina, 2011) exhibit three pairs of adhesive glands – two pairs on the upper region and a third on the frontal region of the head – whereas S. pappaterra possesses two pairs – a single pair of glands on the upper region of the head and another on the frontal region. Jones ]]>
S. pappaterra is rudimentary, although this was not shown by our study. Within the family Cichlidae, S. ]]>
differs from O. niloticus (Nakatani et al., 2001; Fujimura & Okada, 2007) by the lack of adhesive glands. In sedentary species and those with parental care, these organs play a protective role by preventing the dispersal of larvae, leading to better parental care. Meijide and Guerrero (2000) reported that within their first five days, C. dimerus larvae attach themselves to substrates using mucous secretions released by their ]]>
S. pappaterra, these organs are likely used by larvae to attach themselves within the mouth of their parent when threatened.
Myomere number is another widely used characteristic in identifying fish larvae, which can be useful up ]]>
Analysis of the morphological ontogeny of S. pappaterra larvae and juveniles revealed that of seven of the nine variables considered (SnL, HH, HL, and BH as well as SPcF, ]]>
S. pappaterra, as described by Cassemiro, Rangel, Pelicice and Hahn (2008).
Finally, with respect to body-related changes, these are likely associated with increased locomotion during development (Kováč et al., 1999). Furthermore, Gatz Jr. (1979) proposed that body height is inversely related to maximal water velocity and directly related to the ability to perform ]]>
S. pappaterra is consistent with the ecological requirements of this species, which primarily occur in structured lentic environments with aquatic macrophytes (Casatti, Mendes, & Ferreira, 2003).
]]>
Acknowledgments
The authors would like to thank the Agreement UEM/ Nupélia//Furnas Centrais Elétricas S.A. for their financial support and the Research Center on Limnology, Ichthyology and Aquaculture (Nupélia) for their logistical support. We would also like to thank the Program of Scientific ]]>
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1. Universidade Estadual de Maringá (UEM), Departamento de Biologia (DBI), Programa de Pós-Graduação em Ecologia de Ambientes Aquáticos Continentais (PEA), Av. Colombo, 5790, CEP 87020-900, Maringá, Paraná, Brazil; taisemlopes@gmail.com, fgoliveira.bio@gmail.com
2. Núcleo de Pesquisa em Ictiologia, Limnologia e Aquicultura (NUPELIA), Av. Colombo, 5790, Bloco H90, CEP 87020-900, Maringá, Paraná, Brazil; bialetzki@nupelia.uem.br, agostinhoaa@nupelia.uem.br
Received 03-IV-2014. Corrected 11-VIII-2014. Accepted 09-IX-2014.