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Revista de Biología Tropical

On-line version ISSN 0034-7744Print version ISSN 0034-7744

Rev. biol. trop vol.62 n.3 San José Jul./Sep. 2014

 

Reproductive tactics optimizing the survival of the offspring of Cichlasoma orientale (Perciformes: Cichlidae)

Tácticas reproductivas para optimizan la supervivencia de la descendencia de Cichlasoma orientale (Perciformes: Cichlidae)

Jussiara Candeira Spíndola Linhares1*, Luisa Resende Manna2*, Rosana Mazzoni2, Carla Ferreira Rezende1 & José Roberto Feitosa Silva1


Abstract

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 towards environmental conditions and ecological niches for which different species have a specific response. The objective of this study was to describe reproductive tactics related to the survival of 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 and focal-animal sampling. Collected individuals (males n=185, females n=95) were evaluated regarding the standard length, batch fecundity, oocyte size and spawning pattern. In females with mature ovaries, oocyte groups at different developmental stages were observed, these cells were counted and measured, and fecundity was estimated by the gravimetric method. Our results showed that the species displayed biparental care behavior and, on average, males were larger than females. Based on 46 ovaries, the average batch fecundity was 2 052±849 (range: 254-3 389). Standard length and batch fecundity were positively correlated, but no correlation was found between oocyte size and standard length. The maximum diameter observed in the most developed oocytes was 1.8mm. The observed distribution of oocyte size classes indicated synchronous oocyte development in three groups: previtellogenic, vitellogenic and mature, showing that 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 increases chances of survival mainly because of increased fecundity per reproductive season, and the reduced competition among the offspring. We concluded  that 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

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 reproductivas relacionadas con la supervivencia de la descendencia de 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 lénticos y lóticos en la cuenca del río Curu, región semiárida del noreste de Brasil. El comportamiento individual (n=113) se observó bajo el agua durante más de 50 horas por un muestreo 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 hembras con ovarios maduros, se observó la cantidad de grupos de ovocitos en diferentes etapas de desarrollo y estas células fueron contadas y medidas y la fecundidad se estimadó por el método gravimétrico. Las especies muestran un comportamiento de cuidado biparental y, en promedio, los machos son más grandes que las hembras. Con base en 46 ovarios, la fecundidad promedio de lotes fue de 2 052±849 (254-3 389). Longitud estándar y fecundidad parcial se correlacionaron positivamente, pero no se encontró correlación entre el tamaño de los ovocitos y la longitud estándar. Los oocitos más desarrollados miden 1.8mm. La distribución observada de las clases de tamaño de los ovocitos indica desarrollo de los ovocitos sincrónico en tres grupos: pre-vitelogénicos, vitelogénicos y maduros, lo que demuestra que C. orientale es una especie con desova múltiple. Se observaron diferencias en la cantidad de ovocitos entre los tres grupos, con el grupo más desarrollada que muestra el menor número de ovocitos. La combinación de la baja fecundidad y gran tamaño del huevo es una característica de los reproductores demersales, debido a una mayor estabilidad del medio ambiente. Múltiples desoves aumenta las posibilidades de supervivencia, principalmente debido al aumento de la fecundidad por temporada reproductiva y reducción de la competencia entre la descendencia. Llegamos a la conclusión de que 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 biparental, reproducción.


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,  depending  on  environmental conditions and ecological niche (Winemiller, 1989; Murua, & Saborido-Rey, 2003).

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, 2013). Teleosts fecundity may be determinate or indeterminate (Hunter, Lo, & Leong, 1985). In the former case, oocyte recruitment is completed before spawning begins; thus, the number of mature oocytes in the ovary corresponds to the poten- tial annual fecundity (Hunter, Macewicz, Lo, & Kimbrell, 1992). In the latter case, oocyte recruitment and spawning overlap; thus, potential fecundity is not determined prior to spawn- ing (Hunter et al., 1992; Fernandes, Oliveira, Travassos & Hazin, 2012).

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  competition and predation (Nikolsky, 1963; McEvoy, & McEvoy, 1992).

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 predators (Zworykin, Budaev & Mochek, 2000).

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, 1989). This author defined three strategies that indicate kinds of reactions to environmental variations. The first is an opportunistic strategy that is developed by small organisms with fast maturation and few eggs. The second is a seasonal strategy, in which species present a high fecundity, short reproductive season and low offspring survival. Concluding the triangular model of strategies, the equilibrium strategy is performed by density dependent species, that perform parental care, exhibit a long reproduc- tive season and low fecundity with large eggs, and generally live in habitats with limited resources (Winemiller, 1989, 1995; Zeug, & Winemiller, 2007).

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 experience a safe habitat during the initial development. This  family  is  naturally  distributed  in  Central and South America, Africa, Middle East, Iran, India and Sri Lanka (Kullander, 2003). The neotropical cichlid species 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 other two sites (3º49’08” S - 39º19’57” W and 3º57’08” S - 39º25’56” W) are lotic environment. In these lotic environments water volume varies greatly through- out the year, according to rain regimes, varying from approximately 6m wide during dry season to 50m wide during rainy season. The semiarid regions of Northeastern Brazil are subject to irregular and sometimes extended drought periods (Krol, Jaegar, Brontert & Krywkow, 2001; Chiang & Coutavas, 2004). Rainfalls vary from 240 to 1 500mm per year, with average temperatures in the range 24-26ºC (Nimer, 1972). The rainy season is characterized by intense showers, usually from March to July (Bouvy, Falção, Marinho, Pagano & Moura, 2000). Most rivers and streams in the region are intermittent, with little or no flow during the dry season (Maltchik, 1999). Due to precipitation variations in the region, the main basins have been modified with a great number of dams built in the main rivers stream beds, which ensures water to all human population in order to accomplish their activities during drought season (Andrade, Araújo, Rosa, Gomes, & Lobato, 2007; Chellappa, Bueno, Chellappa, Chellapa, & val, 2009).

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 sampling, observing a single individual for up to five minutes (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 August 2011 to July 2013 were used to obtain information on standard length, batch fecundity, oocyte  size  and  spawning  pattern.  Fishing gear consisted of seine nets with 0.5mm mesh size and gill nets with 40-100mm mesh size. Sampled individuals were anesthetized with eugenol (concentration = 100mg/L) and euthanized with ice, in accordance with Brazilian environmental legislation (sampling authorized by ICMBio under entry #28 385-2). voucher specimens of 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 oocytes in chromatin nucleolar phase (stage I) and peri-nucleolar (stage II) and in testis primary and secondary spermatogonia are predominantly observed. II – in maturation: ovaries are orange and  it  is  possible  to  observe  some  oocytes with the naked eye, while testis have a whitish color. Histologically it is observed the presence of oocytes in stages I, II and cortical alveoli (stage III) in ovaries and spermatogonia, sper- matocytes and spermatids in testis. Also, at the end of this stage some spermatozoids can be observed in testis lumen. III – mature: macro- scopically ovaries present a color varying from yellow to light brown, and occupy most of the coelomic cavity   and one can easily identify the oocytes with the naked eye, and testis are turgid and whitish. Histologically it can be observed the presence of oocytes in phases I, II, III and mature (stage Iv) in ovaries, and a great number of spermatozoids in the testis lumen. Iv – partially spawned: ovaries and testis are flaccid and it is possible to observe in some cases some hemorrhagic zones. Histologically, ovaries show empty spaces, oocytes in stages I to Iv and atretic and post ovulatory follicles. In testis lumen there are some residual spermatozoids and spermatogonia.

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).

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 met,  regressions  were  performed.  The  type of regression was defined by the highest r² values. The  numbers  of  oocytes  at  different stages of development were compared using the paired t test.

Results

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 categories of behavior were observed (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; p<0.0001) (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 oocytes. 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. Clearly visible to the naked eye, these oocytes vary in color from orange to light brown. Under light microscopy, the cytoplasm appears filled with yolk granules. The nucleus is difficult to locate due to its small size in relation to the oocyte. The number of fully mature oocytes is on the average 20% smaller than the number of vitellogenic oocytes (tpar =180; gl =44; p=0.044). The oocytes in this group are released in the following spawn.

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 three stages described above, 82% of the analyzed ovaries contained whitish and brittle cells identified as atretic oocytes. These varied up to three times in size within the same ovary.

Discussion

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, Coward, Bromage, 2004). Teleosts fecundity vary greatly regardless of size (Mazzoni & Caramaschi,  1997;  Serezli,  Guzel,  &  Kocabas, 2010;  Casimiro,  Garcia,  Almeida,  &  Orsi, 2011; Juchno & Boroń, 2012; Peressi, Gonçalvez, & Braga, 2012; Fernandes et al., 2012; Trujillo-Jiménez, Sedeño-Diaz, Camargo, & López-López, 2013), indicating the existence of an array of reproductive tactics, concentrating resources on the production of either many and small or few and large eggs (Wooton, 1984, Casimiro et al., 2011). The relation between size and number is among other things associated with the habitat in which spawning takes place (Duarte & Alcaraz, 1989). According to these authors, larval mortality among pelagic spawners is mainly regulated by environmental variability. In the pelagic zone, greater fecundity means more eggs hatching in a favorable habitat, thus greater reproductive success. On the other hand, demersal spawners have more control over the circumstances in which their eggs will hatch, thereby reducing the vari- ability of growth conditions. Thus, because demersal fishes invest more heavily in larval survival, oocytes tend to be larger (Duarte & Alcaraz, 1989).

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 and/or by way of direct parental care during the early stages of life (Winemiller, 1995; Korzelecka-Orkisz et al., 2012).

The  individuals  observed  underwater  in the Curu river basin engaged in biparental care,  
thereby increasing the chances of larval survival. Parental care includes any form of direct protection of the offspring after fertilization (Gross & Sargent, 1985), whether it be the eggs (e.g. nest patrolling) or free-swimming larvae and juveniles (e.g. accompanying juveniles) (Baylis, 1981). Larger eggs are associated with increased  survival  potential  as  larger  larvae are subject to lower mortality rates (McGurk, 1986): they feed on larger food items, swim faster and carry larger amounts of yolk with which to resist periods of food scarcity while searching for a favorable habitat (Duarte & Alcaraz, 1989). Larger larvae are also easier to defend from predators (Souza, Fragoso-Moura, Freneich-verani, Rocha & verani, 2008). The elliptical shape of the oocytes 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 (Kume & Joseph, 1966)  and  longevity  (Wu,  Su,  &  Kawasaki, 2001). Usually, a larger body volume would allow the female to allocate more eggs and therefore might be considered an evolutionary advantage (Moraes et al., 2013). In Cichlidae, however, males tend to be larger than females (Garcia-Lizárraga et al., 2011, Araújo et al., 2012), possibly because larger males protect the offspring more efficiently, thereby ensuring greater reproductive success (Keenleyside, 1991). Likewise, while both parents of the cichlid species Laetacara araguaiae patrol the nest, the male displays more developed parental behaviors, especially in the premating stage and when guarding eggs and larvae (Teresa & Gonçalves-de-Freitas, 2011). Size also seems to make a significant difference in courtship. Experiments with the cichlid species 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; Reid & Chaput, 2012). The correlation may be explained by the fact that larger individuals have more energy available for the production of oocytes (Patimar & Mohammadzadeh, 2011) and larger females have more space in the abdominal cavity, providing greater fecundity.

In many teleosts, when analyzed intra-specifically, egg size and standard length are positively correlated: older and larger females tend to produce larger oocytes, increasing chances of larval survival (Rana, 1988; Kjesbu, 1989; Reid & Chaput, 2012). However, no such correlation was observed in the present study, matching reports for other species of cichlids (Rana, 1988; Coward & Bromage, 1999) and for some species of teleosts (Rodrigues & Macchi, 2010; Peressin et al., 2012). Within a given population, egg size may be influenced by detrimental habitat changes (Hainfellner, Souza, Moreira, Makaghi, & Batlouni, 2012) or by the number of previous spawns in the reproductive cycle (oocytes tend to be larger in the first spawns) (Kjesbu, 1989).

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  of  the  offspring may develop under ideal conditions (Growns, 2004), and iii) it reduces competition between larvae/juveniles and predation of eggs and larvae (McEvoy & McEvoy, 1992). Many ciclids  are  multiple  spawners  (Winemiller, 1989; Coward & Bromage, 1999; Paugy, 2002; Campos-Mendonza et al., 2004; Araújo et al., 2012; Korzelecka-Orkisz et al., 2012); in such species, fecundity is high (considering the length of the reproductive period) and survival is favored as larval competition is minimized.

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 with atretic oocytes. Thus, in females with limited energy reserves, oocyte development may be interrupted, there- by regulating the number of eggs produced (McEvoy & McEvoy, 1992), generating just the ideal number to the conditions the environment presents at that moment. The seasonal environment of the semiarid region may yet be of great influence in the great amount of females found carrying atretic oocytes due to drastic variation in water level and consequent availability of mesohabitats to build nests.

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 care and multiple spawning pattern.

Acknowledgments

This study is part of the Ph.D. thesis of the principal author (CAPES-REUNI). We would like to thank the members of Laboratório de Ecologia de Rios do Semiárido, Universidade Federal do Ceará, for assistance with field work, víctor Távora for the illustrations of behaviors, Cynthia Ogawa for the translation to English, and Leonardo Peres de Souza for help- ing with the histological analysis and review of the manuscript.


References

Araújo, A. S., Nascimento, W. S., Yamamoto, M. E., & Chellappa, S. (2012). Temporal dynamics of reproduction of the neotropical fish, Crenicichla menezesi (Perciformes: Cichlidae). The Scientific World Journal, 2012, 1-10.         [ Links ]

Andrade, E. M., Araújo, L. F. P., Rosa, M. F., Gomes, R. B., & Lobato, F. A. (2007). Fatores determinantes da  qualidade  das  águas  superficiais  na  bacia  do Alto Acaraú,  Ceará,  Brasil.  Ciência  Rural,  37(6), 1791-1797.         [ Links ]

Bagenal, T. G. (1967). A short review of fish fecundity. In S. D. Gerking (Ed.), The biological basis of freshwater fish production (pp. 89-111). New York: John Wiley.         [ Links ]

Baylis, J. R. (1981). The evolution of parental care in fishes, with reference to Darwin’s rule of sexual selection. Environmental Biology of Fishes, 6(2), 233-251.         [ Links ]

Boussou, C. K., Edia, E. O., Konan, F. K., Ouattara, M., Ouattara,  A.,  &  Gourène,  G.  (2010).  Reproducti- ve  biology  of  Chromidotilapia  guntheri  (Sauvage, 1882) (Cichlidae, Perciformes) in four coastal rivers (Ehania, Noé, Soumié and Eholié) of Côte d’Ivoire in West Africa. Knowledge and Management of Aquatic Ecosystems, 396(3), 1-16.         [ Links ]

Bouvy,  M.,  Falção,  D.,  Marinho,  M.,  Pagano,  M.,  & Moura, A. (2000). Occurrence of Cylindrospermopsis (Cyanobacteria) in 39 Brazilian tropical reservoirs during the 1998 drought. Aquatic Microbial Ecology, 23, 13-27.         [ Links ]

Byskov, A. (1978). Follicular atresia. In R. E. Jones (Ed.), The vertebrate ovary (pp. 533-562). New York: Plenum Press.         [ Links ]

Cacho, M. S. R. F., Yamamoto, M. E., & Chellappa, S. (2007). Mating system of the amazonian cichlid angel fish, Pterophyllum scalare. Brazilian Journal of Biology, 67(1), 161-165.         [ Links ]

Campos-Mendoza,  A.,  McAndrew,  B.  J.,  Coward,  K., &  Bromage,  N.  (2004).  Reproductive  response  of Nile tilapia (Oreochromis niloticus) to photoperiodic manipulation; effects on spawning periodicity, fecundity and egg size. Aquaculture, 231(1-4), 299-314.         [ Links ]

Casimiro, A. C. R., Garcia, D. A. Z., Almeida, F. S., & Orsi, M. L. (2011). Reproductive aspects of Moenkhausia intermedia Eigenmann, 1908 (Pisces, Characidae) in the Upper Paraná River Basin, Brazil. ISRN Zoology, 2011, 1-8.         [ Links ]

Chávez-López, R., Peterson, M. S., Brown-Peterson, N. J., Morales-Gómez, A. A., & Franco-López, J. (2005). Ecology of the Mayan Cichlid, Cichlasoma urophthalmus Günther, in the Alvarado Lagoonal System, veracruz,  Mexico.  Gulf  and  Caribbean  Research, 16(2), 1-10.         [ Links ]

Chellappa, S., Bueno, R. M. X., Chellappa, T., Chellappa, N. T., & val, v. M. F. A. (2009). Reproductive seasonality of the fish fauna and limnoecology of semi-arid Brazilian reservoirs. Limnologica, 39(4), 325-329.         [ Links ]

Chiang, J. C. H. & Koutavas, A. (2004). Tropical flip-flop connections. Nature, 432, 684-685.         [ Links ]

Coward, K., & Bromage, N. R. (1999). Spawning periodicity, fecundity and egg size in laboratoru-held stocks of a substrate-spawnig tilapiine, Tilapia zillii (Gervais). Aquaculture, 171(3-4), 251-267.         [ Links ]

Duarte, C. M. & Alcaraz, M. (1989). To produce many small or few large eggs: a size-independent reproductive tactic of fish. Oecologia, 80(3), 401-404.         [ Links ]

Fernandes, C. A. F, Oliveira, P. G. v., Travassos, P. E. P., & Hazin, F. v. H. (2012). Reproduction of the Brazilian snapper,  Lutjanus  alexanderi  Moura  &  Lindeman, 2007 (Perciformes: Lutjanidae), off the northern coast of Pernambuco, Brazil. Neotropical Ichthyology, 10(3), 587-592.         [ Links ]

Ganias, K. (2013). Determining the indeterminate: Evolving  concepts  and  methods  on  the  assessment  of the fecundity pattern of fishes. Fisheries Research, 138, 23-30. Retrieved from http://www.sciencedirect. com/science/article/pii/S0165783612001622.   doi: 10.1016/j.fishres.2012.05.006.         [ Links ]

Garcia-Lizarraga, M. A., Soto-Franco, F. E., Jesús J. M., velazco-Arce, R., velázquez-Abunader, J. I., Ramí- rez-Pérez, J. S., & Peña-Messina, E. (2011). Population structure and reproductive behavior of Sinaloa cichlid Cichlasoma beani (Jordan, 1889) in a tropical reservoir. Neotropical Ichthyology, 9(3), 593-599.         [ Links ]

Gross, M. R. & Sargent, R. C. (1985). The evolution of male and female parental care in fishes. American Zoologist, 25(3), 807-822.         [ Links ]

Growns, I. (2004). A numerical classification of reproductive guilds of the freshwater fishes of south-eastern Australia and their application to river management. Fisheries Management and Ecology, 11(6), 369-377.         [ Links ]

Hainfellner, P., Souza, T. G., Moreira, R. G., Nakaghi, L. S. O., & Batlouni, S. R. (2012). Gonadal steroids levels and vitelogenesis in the formation oocytes in Prochilodus lineatus (valenciennes) (Teleostei: Characiformes). Neotropical Ichthyology, 10(3), 601-612.         [ Links ]

Hunter, J. R., Macewicz, B. J., Lo, N. C. H., & Kimbrell, C. A. (1992). Fecundity, spawning, and maturity of female Dover Sole, Microstomus pacificus, with an evaluation of assumptions and precision. Fishery Bulletin, 90, 101-128.         [ Links ]

Hunter, J. R., Lo, N. C. H., & Leong, R. J. H. (1985). Batch fecundity in multiple spawning fishes, In R. Lasker (Ed.), An egg production method for estimating spawning biomass of pelagic fish: application to the northern anchovy Engraulis  ordax (pp. 67-78). NOAA Tech. Rep. NMFS-36.         [ Links ]

Juchno, D. & Boroń, A. (2012). Reproduction and fecundity of the golden loach, Sabanejewia baltica Witkowski, 1994 from Bug River in Poland. Reproductive Biology, 12(1), 73-79.         [ Links ]

Junqueira, L. C. & Junqueira, L. M. M. S. (1983). Técnicas Básicas de Citologia e Histologia. São Paulo: Livraria e Editora Santos.         [ Links ]

Keenleyside, M. H. A. (1991). Parental care. In M. H. A Keenleyside (Ed.), Cichlid fishes: behaviour, ecology and evolution. (pp. 191-208). London: Chapman & Hall.         [ Links ]

Keenleyside, M. H. A. (1991b). Cichlid fishes: behaviour, ecology and evolution. London: Chapman & Hall.         [ Links ]

Kjesbu, O. S. (1989). The spawning activity of cod, Gadus morhua L. Journal of Fish Biology, 34(2), 195-206.         [ Links ]

Kjesbu, O. S., Hunter, J. R., & Witthames, P. R. (2003). Report on the working group on modern approaches to assess maturity and fecundity of warm-and cold- water fish and squids. Bergen. Retrieved from https:// www.imr.no/filarkiv/2003/12/NR.12_2003_Modern_ approaches_to_assess_maturity_and_fecundity_of_warm-_and_cold-water_fish_and_squids.pdf/nb-no.         [ Links ]

Korzelecka-Orkisz, A., Szalast, Z., Pawlos, D., Smaruj, I., Tañski, A., Szulc, J., & Formicki, K. (2012). Early ontogenesis of the angelfish, Pterophyllum scalare Schultze, 1823 (Cichlidae). Neotropical Ichthyology, 10(3), 567-576.         [ Links ]

Krol,  M.  S.,  Jaegar, A.,  Bronstert, A.,  &  Krywkow,  J. (2001). The semiarid integrated model (SDIM), a regional integrated model assessing water availability, vulnerability of ecosystems and society in NE-Brazil. Physics and Chemistry of the Earth, 26(7-8), 529-533.         [ Links ]

Kullander,  S.  O.  (2003).  Family  Cichlidae  (Cichlids). In R. E. Reis, S. O. Kullander, C. J. JR. Ferraris (Eds.), Check List of the Freshwater Fishes of South and Central America (p. 605-654). Porto Alegre: Edipucrs.         [ Links ]

Kume, S. & Joseph, J. (1966). Size composition, growth and sexual maturity of bigeye tuna, Thunnus obesus (Lowe), from the Japanese long-line fishery in the eastern Pacific Ocean. Inter-American Tropical Tuna Commission Bulletin, 11(2), 45-99.         [ Links ]

Lehner, P. N. (1996). Handbook of Ethological Methods. United Kingdom: Cambridge University Press.         [ Links ]

Lowe-McConnell, R. H. (1969). The cichlid fishes of Guyana, South America, with notes on their ecology  and  breeding  behaviour.  Zoological  Journal  of the Linnean Society, 48(2), 255-302.         [ Links ]

MacArthur, R. H. & Wilson, E. O. (1967). The Theory of Island Biogeography. Princeton: Princeton University Press.         [ Links ]

Maltchik, L. (1999). Ecologia de rios intermitentes tropicais. In M. L. M. Pompeo (Ed.), Perspectivas da limnologia no Brasil (pp. 77-89). São Luís: Gráfica e editora União.         [ Links ]

Martinez-Palacios, C. A. & Ross, L. G. (1992). The reproductive biology and growth of the Central American cichlid Cichlasoma urophthalmus (Günther). Journal of Applied Ichthyology, 8(1-4), 99-109.         [ Links ]

Mazzoni, R. & Iglesias-Rios, R. (2002). Environmentally related life history variations in Geophagus brasiliensis. Journal of Fish Biology, 61(6), 1606-1618.         [ Links ]

Mazzoni, R. & Caramaschi, E. P. (1997). Observations on the reproductive biology of female Hypostomus luetkeni Lacèpéde 1803. Ecology of Freshwater Fish, 6(1), 53-56.         [ Links ]

McEvoy, L. A. & McEvoy, J. (1992). Multiple spawning in several commercial fishes and it’s consequences for fisheries management, cultivation and experimentation. Journal of Fish Biology, 41(Issue Supplement), 125-136.         [ Links ]

McGurk, M. D. (1986). Natural mortality of marine pelagic fish eggs and larvae: role of spatial patchiness. Marine Ecology Progress Series, 34, 227-242.         [ Links ]

Moraes, M., Filho, J. J. S., Costa, R., Miranda, J. C., Rezende, C. F., & Mazzoni, R. (2013). Life history and ontogenetic  diet  shifts  of  Pimelodella  lateristriga (Lichtenstein 1823) (Osteichthyes, Siluriformes) from a coastal stream of Southeast Brazil. North-Western Journal of Zoology, 9(2), 1-10.         [ Links ]

Murua, H. & Saborido-Rey, F. (2003). Female reproductive strategies of marine fish species of the North Atlantic. Journal of Northwest Atlantic Fishery Science, 33, 23-31.         [ Links ]

Nikolsky, G. v. (1963). The ecology of fishes. London: Academic Press.         [ Links ]

Nimer, E. (1972). Climatologia da região Nordeste do Brasil. Introdução à climatologia dinâmica. Revista Brasileira de Geografia, 34(1), 3-48.         [ Links ]

Ortega-Salas, A. A., Cortés, I., & Reyes-Bustamante, H. (2009). Fecundity, growth, and survival of the angel-fish Pterophyllum scalare (Perciformes: Cichlidae) under laboratory conditions. Revista de Biologia Tropical, 57(3), 741-747.         [ Links ]

Patimar, R. & Mohammadzadeh, B. (2011). On the biological  characteristics  of  Capoeta  fusca  Nikolskii, 1897 in eastern Iran. Journal of Applied Ichthyology, 27(3), 873-878.         [ Links ]

Paugy, D. (2002). Reproductive strategies of fishes in a tropical temporary stream of the Upper Senegal basin: Baoulé  River  in  Mali.  Aquatic  Living  Resources, 15(1), 25-35.         [ Links ]

Peressin, A., Gonçalves, C. S., & Braga, F. M. S. (2012). Reproductive strategies of two Curimatidae species in a Mogi Guaçu impoundment, upper Paraná River basin,  São  Paulo,  Brazil.  Neotropical  Ichthyology, 10(4), 847-854.         [ Links ]

Pianka, E. R. (1970). On r- and K-Selection. The American Naturalist, 104(940), 592-597.         [ Links ]

Rana, K. J. (1988). Reproductive biology and the hatchery rearing of tilapia eggs and fry. In J. F. Muir & R. J. Roberts (Eds.), Recent Advances in Aquaculture (pp. 343-406). Longon: Croom Helm.         [ Links ]

Reid, J. E. & Chaput, G. (2012). Spawning history influence on fecundity, egg size, and egg, survival of Atlantic salmon (Salmo salar) from the Miramichi River, New Brunswick, Canadá. Journal of Marine Science, 69(9), 1678-1685.         [ Links ]

Reznick, D. (1985). Costs of reproduction: an evaluation of the empirical evidence. Oikos, 44(2), 257-267.         [ Links ]

Rickman, S. J., Dulvy, N. K., Jennings, S., & Reynolds, J. D. (2000). Recruitment variation related to fecundity in marine fishes. Canadian Journal of Fisheries and Aquatic Sciences, 57(1), 116-124.         [ Links ]

Rodrigues,  K.  A.  &  Macchi,  G.  G.  (2010).  Spawning and  reproductive  potential  of  the  Northern  stock of Argentine hake (Merluccius hubbsi). Fisheries Research, 106(3), 560-566.         [ Links ]

Sabino, J. (1999). Comportamento de peixes de riachos brasileiros: métodos de estudos para uma abordagem naturalística. In E. P. Caramaschi, R. Mazzoni, & P. R. Peres-Neto (Eds.), Ecologia de Peixes de Riachos, Série Oecologia Brasiliensis (pp. 183-208). Rio de Janeiro: Computer & Publish Editoração Ltda.         [ Links ]

Serezli, R., Guzel, S., & Kocabas, M. (2010). Fecundity and egg size of three salmonid species (Oncorhynchus mukiss, Salmo labrax, Salvelinus fontinalis) cultured at the same farm condition in North-Eastern, Turkey. Journal of Animal and Veterinary Advances, 9(3), 576-580.         [ Links ]

Souza, J. E., Fragoso-Moura, E. N., Freneich-verani, N., Rocha, O., & verani, J. R. P. (2008). Population structure and reprodutive biology of Cichla kelberi (Perciformes, Cichlidae) in Lobo Reservoir, Brazil. Neotropical Ichthyology, 6(2), 201-210.         [ Links ]

Stearns, S. C. (1976). Life-history tactics: a review of the ideas. The Quaterly Review of Biology, 51(1), 3-47.         [ Links ]

Teresa, F. B. & Gonçalves-de-Freitas, E. (2011). Reproductive  behavior  and  parental  roles  of  the  cichlid fish Laetacara araguaiae. Neotropical Ichthyology, 9(2), 355-362.         [ Links ]

Townshend, T. J. & Wootton, J. (1984). Effects of food supply on the reproduction of the convict cichlid, Cichlasoma nigrofasciatum. Journal of Fish Biology, 24(1), 91-104.         [ Links ]

Trujillo-Jiménez, P., Sedeño-Díaz, J. E., Camargo, J. A., & López-López, E. (2013). Reproductive traits and population structure of Astyanax aeneus (Characiformes: Characidae) from a subtropical river in Mexico. Revista de Biologia Tropical, 61(2), 769-786.         [ Links ]

Winemiller, K. O. (1989). Patterns of variation in life history  among  South American  fishes  in  seasonal environments. Oecologia, 81(2), 225-241.         [ Links ]

Winemiller, K. O. (1995). Fish ecology. In W. A. Nieren- berg (Ed.), Encyclopedia of Environmental Biology (pp. 49-65). San Diego: Academic Press.         [ Links ]

Wooton, R. J. (1984). Introduction: Strategies and tactics in fish reproduction. In G. W. Potts & R. J. Wooton (Eds.), Fish reproduction: strategies and tactics (pp. 1-12). Oxford: Academic Press.         [ Links ]

Wu, C. C., Su, W.C., & Kawasaki, T. (2001). Reproductive biology of the dolphin fish Coriphaena hippurus on the east coast of Taiwan. Fisheries Science, 67(5), 784-793.         [ Links ]

Zeug, S. C. & Winemiller, K. O. (2007). Ecological correlates of fish reproductive activity in floodplain rivers: a life history-based approach. Canadian Journal of Fisheries and Aquatic Sciences, 64(10), 1291-1301.         [ Links ]

Zworykin, D. D., Budaev, S. v., & Mochek, A. D. (2000). Does parental fin digging improve feeding opportunities for offspring in the convict cichlid? Environmental Biology of Fishes, 57(4), 443-449.         [ Links ]

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.

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