High mortality rates have been observed in Teleost during early developmental stages, as well as great variations in reproductive tactics, which are related to adaptations ]]>
Cichlasoma orientale offspring, including aspects of body size, parental care, fecundity, oocyte size and spawning patterns. Samples were performed monthly from August 2011 to July 2013, in lentic and lotic environments at Curu river basin, Brazilian Northeastern semiarid region. Individual behavior (n=113) was observed underwater for over 50 hours by ad libitum sampling ]]>
C. orientale is a multiple spawner. Differences in the amount of oocytes among the three groups were observed, with the most developed group showing the smallest number of oocytes. The combination of low fecundity and large egg size is characteristic of demersal spawners due to a greater environmental stability. Multiple spawning ]]>
C. orientale makes a heavy investment in larval survival in detriment of the offspring number. Survival is favored by the large size of oocytes, large yolk reserve, biparental care and multiple spawning pattern. ]]>
Key words: fecundity, oocyte size, multiple spawning, biparental care, reproduction.
Resumen
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Las altas tasas de mortalidad se han observado en teleósteos durante las etapas iniciales del desarrollo, así como una gran variación en las tácticas reproductivas, que están relacionados con adaptaciones a las condiciones ambientales y nichos ecológicos con cada especie que presenta una respuesta específica. El objetivo de este estudio fue describir las tácticas ]]>
Cichlasoma orientale, incluyendo aspectos tales como el tamaño corporal, el cuidado parental, la fecundidad, el tamaño de los ovocitos y los patrones de desove. Las muestras se recolectaron mensualmente desde agosto 2011 hasta julio 2013, en ambientes ]]>
ad libitum y muestreo de grupos focales. Para los individuos recolectados (n=185 machos, hembras n=95) se evaluó: la longitud, la fecundidad por camada, el tamaño estándar de los ovocitos y el patrón de desove. En las ]]>
C. orientale es una especie con desova múltiple. Se observaron diferencias en la cantidad de ovocitos entre los tres ]]>
C. orientale hace una fuerte inversión en la supervivencia de las larvas en detri- mento del número de descendientes. La supervivencia se ve favorecida por el gran tamaño de los ovocitos, gran reserva de yema de huevo, cuidado biparental y patrón de desove múltiple.
Palabras clave: fecundidad, tamaño de los ovocitos, desoves múltiples, cuidado ]]>
Teleosts make large investments in reproduction (Duarte, & Alcaraz, 1989) due to high mortality rates in early stages of life (McGurk, 1986). Offspring survival is safeguarded thanks to a range of reproductive tactics involving fecundity, egg size, spawning patterns and parental care, ]]>
Fecundity plays an important role in recruitment (Rickman, Dulvy, Jennings & Reynolds, 2000) and is regulated by environmental conditions, food availability, predation and genetic factors (Kjesbu, Hunter, & Witthames, 2003; Ganias, ]]>
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Recruitment is also dependent on egg size and spawning pattern. Thus, egg size is inversely proportional to fecundity (Reznick, 1985; Winemiller, 1995) and is a major deter- mining factor of larval quality, with consider- able impact on survival rates (McGurk, 1986). The spawning pattern is characterized by the number of batches per reproductive season and the duration of the season. These aspects have an influence on the number of eggs generated per season and on larval ]]>
Parental care increases substantially the quality of embryonic development and the chances of offspring survival (Korzelecka- Orkisz et al., 2012). Depending on the species, parental care may be provided by the female or the male, or both (Gross & Sargent, 1985). This behavior comprises a range of protective tactics, from aerating to guarding eggs and larvae against ]]>
Environment may influence tactics developed by a certain species to ensure its off- spring survival, with each species presenting a specific response to environmental changes (Stearns, 1976; Winemiller, 1989). This was evidenced in a study that evaluated how species presented changes in their reproductive characteristics in a seasonal environment (Winemiller, ]]>
Among teleostean taxons, Cichlidae dis- plays one of the greatest variations in reproduc- tive strategies (Lowe-McConnell, 1969) with a highly variable fecundity (Araújo, Nascimento, Yamamoto, & Chellappa, 2012). This family invests great amount of energy in offspring survival, presenting parental care, which is performed by one or both genitors (Lowe- McConnel, 1969), and building nests that are the characteristics that allow eggs to ]]>
Cichlasoma orientale Kullander 1983, object of the present study, is considered endemic to Brazilian semiarid regions (Kullander, 2003). ]]>
The objective of this study was to describe reproductive tactics related to offspring survival of Cichlasoma orientale, including aspects of body size, parental care, fecundity, egg size and spawning patterns, based on a population observed in the Curu river basin, Northeastern Brazil.
Materials and methods
Sampling was performed at the Curu river basin in three sites. The first site (3º47’03” S - 39º24’46” W) presents lentic characteristics due to a dam and the ]]>
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The description of parental behavior was based on 50 hours and 24 minutes of underwater observations covering a 100m stretch of Curu river from November 2011 to April and September 2012. Data were collected by ad libitum sampling (Lehner, 1996) and focal-animal ]]>
(sensu Sabino, 1999). Behaviors were classified into four categories (agonistic, offspring protection, nest patrolling, and pair formation) and quantified by a single stationary diver (LRM), far enough (approx. 2m) from observed individuals to not interfere with their behavior (Sabino, 1999).
Individuals sampled monthly from ]]>
C. orientale
were deposited in the fish collection at the Federal University of Paraíba (UFPB 7 067; UFPB 7 081).
In the laboratory, individuals were mea- sured (standard length in cm) and dissected to determine sex and gonadal maturation stage. Gonads were classified into I – immature: very small gonads and translucent, characteristic of young individuals that have not reproduced yet. Histologically ovaries present only ]]>
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Ovaries containing mature oocytes were preserved in Gilson´s fluid for oocyte dissociation (Bagenal, 1967), and after dissociation they were washed and preserved in ethanol 70% for subsequent measurement and count under a stereomicroscope (Hunter et al., 1985). Spawning was inferred based on histological observations of 76 ovaries from different stages (in maturation, mature, and partially spawned) considering oocyte size class.
For histology, ovary samples were immersed in Karnovsky´s fixative for 24 hours, dehydrated in a series of increasing alcohol concentrations, embedded in resin (Leica), sectioned in 3µm sections and stained with hematoxylineosin (adapted from Junqueira, & Junqueira, 1983).
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The batch fecundity was estimated gravi- metrically based on the most developed oocytes (oocytes larger than 900µm), as proposed by Hunter et al. (1985) for species with indeterminate fecundity. The oocytes of three subsamples, corresponding to approximately 10% of the total gonad weight, of each ovary were counted. Based on the number of oocytes in each subsample, the total number of oocytes at each development stage was estimated, and average values were calculated for the ovary. ]]>
Sexes were compared with regard to standard length using the Mann-Whitney test for variables without normal distribution or homoscedasticity. The association between standard length, batch fecundity and oocyte size was evaluated with Pearson´s correlation test. Whenever correlations were significant (p< 0.05), the residues were tested for normality (Shapiro test) and homoscedasticity (Goldfeld- Quandt test). Once these assumptions were ]]>
Results
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A total of 113 individuals of C. orientale were observed underwater. The fish remained mostly in still waters near the river bank, in groups of up to five individuals.
Four different ]]>
Fig. 1). Agonistic behavior, the most frequently observed category (56.52%), was defined as persecuting any other fish, regard- less of species. Pair formation, the second most frequently observed category (26.09%), was defined as swimming together as a pair for up to five minutes with some form of reproductive interaction. Protecting the offspring (pair encircling group of juveniles) was observed three times (13.04%). Patrolling the nest (adult guarding leaf covered with eggs) was observed only once (4.35%). ]]>
Standard length analysis, batch fecundity, oocyte size and spawning pattern was based on 185 males and 95 females collected for the study. Median standard length was 11.91cm (range: 4.01-16.22) for males and 9.55cm (range: 4.07-13.87) for females. Thus, males were larger than females (U=4 518.000; p<0.0001) (Fig. 2). ]]>
Almost half the females (46/95) carried mature oocytes. These females were present in all months of the year (Fig. 3). The mean standard length of females carrying mature oocytes was 10.38cm (range: 4.34-12.80). Batch fecundity was 2 052±849 on the average (range: 254-3 389). The two parameters (batch fecundity and standard length) were directly related when analyzed by power function regression (r=0.87; t=11.53; gl=44; ]]>
Fig. 4). The oocytes of C. orientale are elliptical (measurements refer to the greatest diameter).
•
Previtellogenic oocytes. Size <150μm. Under a stereomicroscope, these oocytes appear whitish. Under light microscopy, the cytoplasm is characterized by intense, homogenous basophilia. Average number of previtellogenic oocytes per ovary: 10 570±4 813.
• Vitellogenic ]]>
Average size 400μm (range: 250-500). These oocytes are orange-colored when observed macroscopically. Under light microscopy, yolk granules are visible, especially in the peripheral cytoplasm. Average number of vitellogenic oocytes per ovary: 2 550±1 087.
• Mature oocytes. Size ≤1.8mm. ]]>
par =180; gl =44; p=0.044). The oocytes in this group are released in the following spawn.
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The oocytes at the same maturation stage varied very little in size within each ovary, but variation was somewhat greater between different individuals, especially with regard to mature oocytes. The latter measured as little as 900μm in less developed ovaries, and up to 1 800μm in more developed ovaries. No correlation was found between oocyte size and standard length (r=0.22; t=1.19, p=0.20).
In addition to the ]]>
Discussion
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Compared to most Teleosts, C. orientale produces few and large oocytes. This pattern has been observed for other species in this genus (Townshend & Wootton, 1984; Martinez-Palacios, & Ross, 1992; Chavez-Lopes, Peterson, Brown-Peterson, Morales-Gómez, & Franco-López, 2005) and family (Coward & Bromage, 1999; Campos-Mendoza, McAndrew, ]]>
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The demersal spawning pattern observed for C. orientale (few and large eggs) indicated that the species invests heavily in larval survival. Indeed, C. orientale also engages in biparental care, as observed for many other cichlids (Winemiller, 1995; Teresa & Gonçalves-de-Freitas, 2011; Korzelecka-Orkisz et al., 2012). These characteristics are associated with the equilibrium strategy guild proposed by Winemiller (1989), which to a large extent coin- cides with the K strategy for adaptation to life in resource-poor or density-dependent environ- ments (MacArthur & Wilson, 1967; Pianka, 1970). The species in this guild make great efforts to ensure the survival of their offspring by providing them with significant amounts of yolk ]]>
The individuals observed underwater in the Curu river basin engaged in biparental care, thereby increasing the chances of ]]>
C. orientale makes it possible to deposit eggs in smaller clusters, facilitating patrolling and aeration (Korzelecka-Orkisz et al., 2012). Several species of cichlids have elliptical eggs, with similar benefits (Coward & Bromage, 1999; Korzelecka-Orkisz et al., 2012).
C. orientale differs from the majority of teleosts by the larger size of the male. These differences in sexual ratio have been explained by different hypothesis, such as physiological differences between sexes, mechanisms that makes males more inclined to be captured or less inclined to natural mortality (Boussou et al., 2010), growth rates ]]>
Laetacara araguaiae ]]>
Pteriphyllum scalare have shown that larger and more aggressive males have more mating opportunities than smaller males (Cacho, Yamamoto, & Chellappa, 2007).
]]>
The positive correlation between batch fecundity and standard length among females of C. orientale has been observed for other fish species (Mazzoni & Iglesias-Rios, 2002; Ortega-Salas, Cortés, & Reyes-Bustamante, 2009; Rodrigues & Macchi, 2010; Serezli et al., 2010; Araújo et al., 2012; Peressin et al., 2012; ]]>
In many teleosts, when analyzed intra-specifically, egg size and standard length are positively correlated: older and larger females tend to produce larger oocytes, ]]>
]]>
Even in mature ovaries, oocytes continue to grow due to constant vitellogenesis. The ovaries examined to estimate batch fecundity were considered mature, but oocytes in the third stage of maturation displayed different stages of development according to the proximity of spawning. Further investigations determining oocyte size at the moment of spawning are required to confirm the absence of a correlation between oocyte size and standard length in C. orientale.
Group-synchronous oocyte development is discernible in the distribution of absolute frequency of oocyte size in C. orientale, indicating the species is a multiple spawner. Teleosts with this spawning pattern usually produce few eggs, several times over several months (Growns, 2004). A common tactic in tropical and subtropical species, multiple spawning increases the survival chances of a species (Nikolsky, 1963; Hunter et al., 1985) and offers several advantages: i) it increases the number of eggs spawned throughout the reproductive period (Nikolsky, 1963), ii) the spawn is exposed to a variety of environmental conditions so that at least some ]]>
]]>
The fact that the number of fully mature oocytes was approximately 20% smaller than the number of vitellogenic oocytes may be explained by atresia. Atretic oocytes have been described for many teleosts species (Byskov, 1978). Cichlids present a complex reproductive behavior which can be influenced by abiotic parameters and environmental dynamics (Keenleyside, 1991b). Environmental characteristics such as diminished amount of food or high predation levels can be associated with a greater amount of females ]]>
]]>
The combination of reproductive tactics observed for Cichlasoma orientale in the Curu river basin shows that the species makes a heavy investment in larval survival in detri- ment of the number of offspring. Survival is favored by the large size of the oocytes, large yolk reserve, biparental ]]>
Acknowledgments
This study is part of the Ph.D. thesis of the principal author (CAPES-REUNI). We would like to thank ]]>
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1. Laboratório de Ecologia de Rios do Semiárido, Universidade Federal do Ceará, Campus do Pici, Centro de Ciências, Bloco 909, 60440-900, Fortaleza, Ceará, Brazil; jussiaralinhares@yahoo.com.br, carlarezende.ufc@gmail.com, jrobertofeitosa@gmail.com 2. Laboratório de Ecologia de Peixes, Instituto de Biologia Roberto Alcantara Gomes, Departamento de Ecologia, Universidade do Estado do Rio de Janeiro, 20550-013, Rio de Janeiro, RJ, Brazil; luisamanna@gmail.com, mazzoni@uerj.br
Received 13-I-2014. Corrected 28-III-2014. Accepted 29-Iv-2014.