Ecuador is considered a biodiversity reservoir especially for the native’s freshwater fish species in the Southeastern Tropical Pacific (Álvarez-Mieles et al., 2013). Nine hundred and fifty-one Ecuadorian native species are recognized and grouped in 22 orders, 72 families, 17 subfamilies and 393 genders which represent the 7.8 % of freshwater species of the world, and a 21 % of the species in South America (Barriga, 2012).

In Ecuador, fisheries contribute with 7 % of the total supply of animal protein, estimated at 391 700 t catches made by capture fisheries in 2011 (Sirén, 2011). These catches are made by artisanal fishers in areas such as rivers, lakes, ponds, lagoons, gorges and dams. Ecuador harbors the largest artisanal and small-scale fisheries with responsible practices and environmentally friendly fishing activities that promote conservation of aquatic resources and ecosystems (Rodriguez et al., 2014). This way, Agbayani, Baticados, Quinitio and Tormon-West (2013) indicated that small-scale aquaculture may contribute with food security in the poorest rural areas, and may promote social cohesion and local endogenous development, and at the same time, may enhance livelihoods and biodiversity conservation. The plan is that the conservation of native fisheries resources can be integrated as an essential part of biodiversity maintenance, and joint efforts between authorities, scientists, and local fishers can work together for the sustainability and management of these aquatic zoogenetic resources.

Currently, the native cichlids in Ecuador have come to risk (García, Tume, & Juárez, 2012), mainly due to the replacement of native species by foreign species such as tilapia, because these have highly invaded most areas, and the high catches of native local resources (Canonico, Arthington, McCrary, & Thieme, 2005).

In order to produce and preserve the native species, the administration state created the Cachari Experimental Station, located in Babahoyo in the province of Los Ríos, where a conservation programme for native species is currently being developed by the Subsecretaría de Acuacultura of Ministerio de Agricultura, Ganadería, Acuacultura y Pesca (MAGAP). According to MAGAP, the cultivation of Cichlasoma festae is becoming more and more popular due to its good growth rate, fecundity, ease of manipulation, ability to grow under suboptimal environmental conditions, disease resistance and good consumer acceptance. The first step in developing a conservation plan of a native resource, is the characterization of the species, knowledge of the allometric relationships and estimating its growth models (Delgadillo-Calvillo et al., 2012).

Currently, very few studies have characterized the growth of C. festae in Ecuador. In fishes, the stock assessment uses biological parameters that influence growth such as the weight and length (Karachle & Stergiou, 2012; Wells, Kohin, Teo, Snodgrass, & Uosaki, 2013; Siddique, Arshad, & Amin, 2015). According to Santos, Gaspar, Vasconcelos and Monteiro (2002), length-weight relationship presents several applications, i.e. fish biology, physiology, ecology and fisheries assessment and management. For fisheries population assessment, management and conservation of native species in Ecuador, a mathematical expression of the mean individual body growth was required, relating the size of the species to its age (Katsanevakis & Maravelias, 2008). Nowadays, different growth models are applied: Von Bertalanffy growth pattern is the most widespread in studies (Von Bertalanffy, 1938), although Gompertz pattern (Gompertz, 1825) and Richard’s growth model (Ricker, 1975) are frequently also applied. On the other side, since cichlid farming practices in Ecuador is a relatively recent activity, there are no specific and formal growth studies for local species. Thus, the aim of this research was to provide an initial characterization of the Cichlasoma festae growth during its juvenile stage under semi-controlled conditions, in order to enhance the conservation of this genetic resource, and to promote a sustainable and reliable fishery production.

MATERIALS AND METHODS

Study area and culture conditions: The study was carried out in the Breeding and Conservation Center for Native Species of the Cachari Experimental Station (1º47’59” S - 79º28’54” W) of the Sub-Secretary of fish farming, from the MAGAP on Babahoyo, province of Los Rios (Ecuador). The climate of this area is tropical with an average temperature of 25 ºC, an annual rainfall of 2 400 mm and a relative humidity of 82 %. A total of 720 juveniles of C. festae of three weeks old were cultured, in net cages fixed in a pond bypass of the Babahoyo River, between September 2014 and February 2015. Since male and female could not be differentiated morphologically, sexing of the sampled fish was not carried out. The net cages were fixed in a surface of 1 m2 and submerged 1 m, and were filled at a density of 20 fish per m2, for a total of 18 net cages fixed. A random sample of five fingerlings per cage was taken every week, and each fish was weighed and measured individually. The following biometric parameters were obtained: total length (L), body width (BW) and body depth (BD) (with an ichthy-meter) and body weight (W) (on a top loading digital balance to an accuracy of 0.1 g) (Santos et al., 2002). The juveniles of C. festae were fed with an extruded concentrate composed by 35 % protein, which was initially administered ad libitum, and then adjusted to 3 % of live weight, according to the nutritional recommendations of MAGAP. The study was carried out according to the Ecuadorian national recommendations for the management of fish, taking into consideration the regulations of animal welfare.

Growth model estimations: Firstly, the normality of the distribution of body weight and total length was verified using a Kolmogorov-Smirnov test. The variability of the individual weights and length was expressed as the coefficient of variation. Growth was modelled using non-linear regression analysis. The estimation of growth parameters was performed from weight after Gómez-Ponce, Granados-Flores, Padilla, López-Hernández, and Núñez-Nogueira (2011) and length following Milatou and Megalofonou (2014). We decided to build a model of growth from the length due to less variability of data. Different growth models were fitted to explain the growth of C. festae according to Barreto, Lessa, Hazin, and Santana (2011): the von Bertalanffy’s growth model (VBGM, von Bertalanffy, 1938); the Gompertz’s growth model (Gompertz, 1825); and the Richard’s growth model (Ricker, 1975). The models were detailed as follows:

VBGM: ;

Gompertz: ;

Richard: ;

where L(t) = length at age t; L∞ = maximal asymptotic length; k = growth coefficient; t0 = theoretical age at which fish has zero length; and b = regression parameters and m = constant.

The different growth models were fitted with iterations by means of the Levenberg-Marquardt method for nonlinear least squares. The selection of the best model took place by using the coefficient of determination (R2), the mean squared error (MSE) and Akaike Criterion (AIC) (Akaike, 1974). AIC is a measure of the quality of a selected statistical model that best fits the data using the maximum likelihood technique, according to the methodology proposed by Katsanevakis and Maravelias (2008). Bias-corrected form (AICC) of AIC was used for model selection as follows:

,

where

;

RSS is the residual sum of squares, n the number of observations and k is the number of estimable parameters. The model with the smallest AICC value (AICC, min) was selected as the best among the models tested. The AIC differences (Di = AICC,i - AICC, min) were computed over all models. Finally, models with differences Di > 10 have essentially no support and might be omitted from further consideration; models with differences Di < 2 have substantial support, while there is considerably less support for model with 4 < Di < 7 (Burnham & Anderson, 2002).

Fulton condition factor (K): Fulton Condition factor (K), which is defined as the well-being of the fish, was calculated using the following equation K = 100 W/L3, where W is total weight, and L is the total length in cm (Froese, 2006). K is a useful tool for monitoring of feeding intensity, age and growth rates (González et al., 2016).

Length-weight relationship: Length-weight (L-W) relationship of C. festae was evaluated using the allometric regression analysis (González et al., 2016; Dantas, de Araújo, Fernandes de Oliveira, Silva, & Costa, 2016). The estimation of L-W relationship was made by the adjustment of an exponential curve to the data expressed in its logarithmic form (Santos et al., 2002). L-W relationship was expressed as W = a Lb, the logarithmic transformation of which fives the linear equation log W = log a + b log L, where, W is the total weight in grams, L is the total length in centimetres, a is constant for the initial growth index and b is the growth coefficient. Constant a and b represent the point at which the regression line intercepts the y axis and the slope of the regression line, respectively. The L-W relationship shows an isometric growth when b = 3. Finally, in order to confirm the values of the constant b (slope of L-W relationship model) they were compared with Student’s t-test (H0: b=3) to detect any significant differences on the L-W relationship.

The level of significance in all cases was considered at P < 0.05. All statistical analyses were done using SPSS v.15.

RESULTS

Growth models estimations: A total of 720 juveniles of C. festae were cultivated during 25 weeks. At the beginning of the study, the average weight and length were 4.99 g (Standard Deviation, SD = 0.13) and 6.3 cm (SD = 0.14), respectively, and the average daily growth was 0.199 g.day-1. At the end of the experiment the average weight and length were 35.71 g (SD = 16.38) and 12.25 cm (SD = 2.32). Both individual distributions of weight (Kolmogórov-Smirnov = 0.11; P = 0.20) and length (Kolmogórov-Smirnov = 0.12, P = 0.145) were adjusted to a normal distribution; but a variability lower than 3 % was found for both weight and length data. From the fourth week of the experiment, the weight coefficient of variation (CV) increased significantly (P < 0.01); these differences remained during the subsequent weeks (P < 0.01) (data no presented). The fish final weight showed a variation of 36 % for the sample as a whole, while lower CV for length was observed in a range between 10 to 20 % (data no presented) with a mean value 15.7 %.

The growth parameters estimated for juveniles of C. festae: See table 1. Von Bertalanffy’s model presented the greater value L∞ (19.758 cm). Likewise, VBGM showed the higher growth constant of all the studied models (0.028.week-1). Finally, only VBGM model described t0 value, which indicates the theoretical age at which fish has zero length (-14.463 weeks). These parameters were used to construct the growth curve of C. festae (Fig. 1).

The coefficient of determination (R2), the mean square error (MSE) and Akaike Criterion (AIC, AICC and the differences Di ) were calculated for each data set in each estimated model, (Table 2). The coefficient of determination is widely used by statisticians as a goodness of fit indicator; which had the upper value for VBGM. Likewise Von Bertalanffy’s model presented the lower SEM. Finally, the lowest AIC values were estimated using VBGM model which was considered the best model describing the growth of C. festae Those were followed by Richard’s model, which reached a very similar AIC value (Di < 2) and the Gompertz’s model ranked fourth with Di > 2.

Fulton condition factor (K): The mean value of the condition factor K was 1.76 (SD =0.26) for the original data (from a range of 0.65 to 3). The coefficient of variation was not high (14.90 %).

Length-weight relationship: L-W relationship was estimated by the function: W = 0.0198 L2.96 (lnW = -3.92 + 2.96 ln(L)) with a coefficient of determination (R2) of 94.7 %; and allometric coefficient (b) lower than 3. The parameter b had a mean value of 2.96 (SD = 0.019), subsequently, the significance was verified considering the value of 3 by the use of a t-test (t-test = 25.7; P < 0.05), therefore, an allometric growth during juvenile stage of C. festae was obtained (Fig. 2).

DISCUSSION

The average daily growth of juveniles of C. festae was lower than those reported for Tilapia nilotica (0.49 day-1) (Gómez-Ponce et al., 2011). At the beginning of the study, variability lower than 3 % was found in both weight and length, similar to Dicentrarchus labrax results of Saillant et al. (2003). The low correlation between weight-length with the width (lower than 0.6), could be referred to a juvenile stage data of Cichlasoma, but not to the final stage, where length and weight increased faster than width (Rodríguez et al., 2014).

The Von Bertalanffy’s growth model was fitted to mean length and growth parameters L(t) = 19.758 (1 - e-0.0028(t+14.46)) with an R2 of 0.68. Studies on Tilapia growth in Mexico obtained 56.83 for L∞ and 0.13 for k (Palacios, 1995). Likewise, Gómez-Ponce et al. (2011) obtained higher values of L∞ and k (L∞ = 28.11 cm; k = 0.33 week-1) for Tilapia. However, no C. festae data were available.

The condition factor K is a useful index to monitor feeding intensity, age, and growth rates in fish (Oni, Olayemi, & Adegboye, 1983). It is strongly influenced by both biotic and abiotic environmental conditions and can be used as an index to assess the status of the aquatic ecosystem in which fish live. The condition factor values of C. festae from the current study (1.76) were lower than those registered by Chukwuemeka, Tsadu, Ayanwale, Erhabor, and Falusi (2014) in Tilapia aurea, Tilapia galileae and Auchenoglanius occidentalis and lower than those reported by Anene (2005) in four cichlid fishes (4.9). However, Fagbuaro, Oso, Olurotimi and Akinyemi (2015) recorded significantly lower values (0.68) in Clarias gariepinus fish. The condition factor K obtained in this study implies that the fish may not have feed to the required level.

The length-weight relationship allowed a closer view of the type of growth of this native species. Santos et al., (2002) defined that the isometric type of growth is when the length and weight increase in the same proportion. According to Delgadillo-Calvillo et al. (2012), in aquaculture, the weight is directly proportional to the cube of its length (b=3); this shows an isometric growth, therefore, if b < 3 the growth is negative allometric, while for value over 3, the allometric is positive. The estimated parameter allometric (b) from the weight-length relationship had the value of 2.96 and the intercept of 0.0198. The results showed that the rate of weight gain is less than the rate of length increase. The L-W relationship showed a growth of negative allometric type, the value of the coefficient was b= 2.96. García et al., (2012) indicated an isometric growth between length and weight for Oreochromis niloticus in Peru. Similar results were published by Kullander (2003) for Cichlidae, where the estimation of b was found between 2.93 and 3.33, and the intercept a was found between 0.00576 and 0.0602. In a similar study by Gómez-Ponce et al. (2011) for Oreochromis niloticus in Mexico, allometric coefficients ranged between 2.5 and 3.5 were shown, giving credence to the results of this study.

Barreto et al. (2011) have studied the fish growth by making captures during different growth stages; they have classified the fishes and later have adjusted the recorded measures to a biologic function of Von Bertalanffy. In this study, a direct method was selected according Dampin, Tarnchalanukit, Chunkao, and Maleewong (2012) which studied the growth model of Oreochromis niloticus in net cages fixed with semi-controlled conditions. Although of various failures in breeding, the productive cycle is beginning to be discovered, and the breeding can be reproduced in semi-controlled conditions for future experimental models, and to be used in aquaculture conservation.

In order to improve the conservation of native species, future studies must be developed by small scale fishers generating synergies with researchers. Since stakeholder participation is importantly directed to environmental decision-making processes, they may support the conservation of these local genetics resources. The benefits of different sectors participation on the water quality governance include not only improved interaction and dialogue, but also mutual exchange of knowledge, transparency in the process, and impulse trust among participants.

Future efforts should include genetic and reproductive characterization, in order to promote an integral conservation plan of this resource in Ecuadorian rivers. The obtained non-linear models such L-W relationship as a growth model, constituted suitable indicators of this fish growth; they are easy to obtain, avoid the direct fish handling and diminish risk factors associated with stress and pathology. Moreover, the growth record from length might be associated to photogrammetry, similar to Perea, García, Acero, Valerio and Gómez (2008) in snails; this indicates a great useful for developing of sustainable and reliable fishery production.

RESUMEN

Relación alométrica y modelos de crecimiento de juveniles de Cichlasoma festae (Perciforme: Cichlidae), una especie nativa de agua dulce en Ecuador. Ecuador se considera la capital pesquera del Pacífico tropical sur-oriental con más de 900 especies nativas. Cichlasoma festae representa una importante especie de agua dulce de gran uso local. Por lo tanto, en este estudio, nuestro objetivo fue caracterizar esta especie durante la etapa juvenil, como primer paso para su conservación y valoración, así como para la preparación de propuestas para el desarrollo rural sostenible y la formulación de planes para una gestión pesquera ambientalmente responsable. El estudio duró 25 semanas y se llevó a cabo la zona ictiohidrográfica de la Provincia de Los Ríos, que representa el 35 % de las especies nativas en Ecuador. Semanalmente, se midieron los parámetros biométricos individuales longitud total (L), ancho corporal (BW) y profundidad corporal (BD) de 90 juveniles de C. festae. El crecimiento se determinó utilizando modelos de regresión biológicos no lineales. La longitud media estándar varió entre 6.30 y 12.25 cm y el peso promedio varió entre 4.99 y 35.71 g. La relación longitud-peso se ajustó a la ecuación lnW = -3.92 + 2.96 ln(L), y la especie presentó crecimiento alométrico negativo. Finalmente, el mejor ajuste para el crecimiento de C. festae fue el modelo de Von Bertalanffy donde L∞ = 19.758 cm, k = 0.028 cm week -1 y t0 = -14.463 week -1. Concluimos que el registro de crecimiento de la longitud podría estar asociado a la fotogrametría como una herramienta para el desarrollo de una producción pesquera sostenible y segura.

Palabras clave: Cichlasoma festae, modelos de crecimiento, alometría, conservación, especies nativas.

REFERENCES

Agbayani, R. F., Baticados, D. B., Quinitio, E. T., & Tormon-West, D. H. (2013). Resiliency of small-holder to climate change and market prices in selected communities in the Philippines. In M. G. Bondad-Reantaso & R. P. Subasinghe (Eds.), Enhancing the contribution of small-scale aquaculture to food security, poverty alleviation and socioeconomic development (pp. 171-179). Rome: FAO.

Akaike, H. (1974). A new look at the statistical model identification. IEEE Transactions on Automatic Control, 19, 716-723.

Álvarez-Mieles, G., Irvine, K., Griensven, A., Arias-Hidalgo, M., Torres, A., & Mynett, A. (2013). Relationships between aquatic biotic communities and water quality in a tropical river-wetland system (Ecuador). Environmental Science and Policy, 34, 115-127.

Anene, A. (2005). Condition factor of four Cichlid species of a man-made lake in Imo State, Southeastern Nigeria. Turkish Journal of Fisheries and Aquatic Sciences, 5, 43-47.

Barreto, R., Lessa, R., Hazin, F., & Santana, F. (2011). Age and growth of the blacknose shark, Carcharhinus acronotus (Poey, 1860) off the Northeastern Brazilian Coast. Fisheries Research, 110, 170-176.

Barriga, R. (2012). Lista de peces de agua dulce e intermareales del Ecuador. Revista Politécnica, 30, 83-119.

Burnham, K., & Anderson, D. (2002). Modelling fish growth: multi-model inference as a better alternative to a priori using von Bertalanffy equation. Fish and Fisheries, 9, 178-187.

Canonico, G. C., Arthington, A., McCrary, J. K., & Thieme, M. L. (2005). The effects of introduced tilapias on native biodiversity. Aquatic Conservation: Marine and Freshwater Ecosystems, 15, 463-483.

Chukwuemeka, V. I., Tsadu, S. M., Ayanwale, V. A., Erhabor, O. F. & Falusi, F. M. (2014). Morphometrics of selected fish species from Tagwai Lake, Minna, Niger State, Nigeria. Advances in Agriculture and Biology, 2, 140-143.

Dampin, N., Tarnchalanukit, W., Chunkao, K., & Maleewong, M. (2012). Fish growth model for Nile tilapia (Oreochromis niloticus) in wastewater oxidation pond, Thailand. Procedia Environmental Sciences, 13, 513-524.

Dantas, D., de Araújo, A., Fernandes de Oliveira, J., Silva, R., & Costa, J. (2016). Population structure and reproduction of a migratory fish Leporinus piau (Characiformes: Anostomidae) in a semiarid tropical reservoir, Brazil. Revista de Biología Tropical, 64, 1369-1381.

Delgadillo-Calvillo, A., Martinez-Palacios, C., Berruecos-Villalobos, J., Ulloa-Arzivu, R., López-Ordaz, R., & Vazquez-Pelaez, C. (2012). Caracterización de la curva de crecimiento en dos especies de pez blanco Chirostoma estor, C. promelas y sus híbridos. Veterinaria México, 43, 113-121.

Fagbuaro, O., Oso, J. A., Olurotimi, M. B., & Akinyemi, O. (2015). Morphometric and meristic characteristics of Clarias gariepinus from controlled and uncontrolled population from Southwestern Nigeria. Journal of Agriculture and Ecology Research International, 2, 39-45.

Froese, R. (2006). Cube law, condition factor and weight–length relationships: history, meta-analysis and recommendations. Journal of Applied Ichthyology, 22, 241-253.

García, A., Tume, J., & Juárez, V. (2012). Determinación de los parámetros de crecimiento de la Tilapia Nilótica (Orechromis niloticus) en un estanque revestido con geomembrana y abastecido con agua de subsuelo. Ciencia y Desarrollo, 15, 47-55.

Gómez-Ponce, M. A., Granados-Flores, K., Padilla, C., López-Hernández, M., & Núñez-Nogueira, G. (2011). Edad y crecimiento del híbrido de tilapia Oreochromisiloticus x Oreochromisaureus (Perciformes: Cichlidae) en la represa Zimapán, Hidalgo, México. Revista de Biología Tropical, 59, 761-770.

Gompertz, B. (1825). On the nature of the function expressive of the law of human mortality and on a new model of determining the value of life contingencies. Philosophical Transactions of the Royal Society B: Biological Sciences, 115, 515-585.

González, M., Rodríguez, J., Angón, E., Martínez, A., García, A., & Peña, F. (2016). Characterization of morphological and meristic traits and their variations between two different populations (wild and cultured) of Cichlasoma festae, a species native to tropical Ecuadorian rivers. Archives Animal Breeding, 59, 435-444.

Karachle, P. & Stergiou, K. (2012). Morphometrics and allometry in fishes (1st ed.). INTECH Open Access Publisher.

Katsanevakis, S., & Maravelias, C. (2008). Modelling fish growth: multi-model inference as a better alternative to a priori using von Bertalanffy equation. Fish and fisheries, 9, 178-187.

Kullander, S. (2003). Family Cichlidae. In R. E. Reis, S. O. Kullander, & C. J. Ferraris, (Eds.), Check list of the freshwater fishes of South and Central America (pp. 605-654). Porto: Edipucrs.

Milatou, N. & Megalofonou, P. (2014). Age structure and growth of bluefin tuna (Thunnus thynnus, L.) in the capture-based aquaculture in the Mediterranean Sea. Aquaculture, 424-425, 35-44.

Oni, S. K., Olayemi, J. Y., & Adegboye, J. D. (1983). Comparative physiology of three ecologically distinct fresh water fishes, Alestes nurse Ruppell, Synodontis schall Bloch and S. schneider and Tilapia zilli Gervais. Journal Fish Biology, 22, 105-109.

Palacios, S. S. (1995). Estudio biológico pesquero de la Tilapia Oreochromis aureus en la presa Adolfo López Mateos (El Infiernillo), Michoacán-Guerrero, México (Tesis de Licenciatura). Universidad Nacional Autónoma de México, México.

Perea, J., García, A., Acero, R., Valerio, D., & Gómez, G. (2008). A photogrammetric methodology for size measurements: Application to the study of weight-shell diameter relationship in juvenile Cantareus aspersus snails. Journal of Molluscan Studies, 74, 209-213.

Ricker, W. (1975). A motion for the retirement of the von Bertalanffy function. Canadian Journal of Fisheries and Aquatic Sciences, 38, 1128-1140.

Rodríguez, J., Moya, A., Medina, M., Gómez, J., Perea, P., Merizalde, D., Rodrigez, J., & García, A. (2014). Modelo de crecimiento del Cichlasoma festae en ríos ecuatorianos. Resultados preliminares. Revista Ciencia y Tecnología, 7, 41-48.

Saillant, E., Fostierc, A., Haffrayd, P., Menua, B., Laureaub, S., Thimoniere, J., & Chatain, B. (2003). Effects of rearing density, size grading and parental factors on sex ratios of the sea bass (Dicentrarchuslabrax L.) in intensive aquaculture. Aquaculture, 221, 183-206.

Santos, M. N., Gaspar, M. B., Vasconcelos, P. V., & Monteiro, C. C. (2002). Weight-length relationship for 50 selected fish species of the Algarve coast (Southern Portugal). Fisheries Research, 9, 289-295.

Siddique, M., Arshad, A., & Amin, S. (2015). Length-weight and length-length relationships of two tropical fish Secutor megalolepis (Mochizuki & Hayashi, 1989) and Rhabdamia gracilis (Bleeker, 1856) from Sabah, Malaysia. Journal of Applied Ichthyology, 31, 574-575.

Sirén, A. (2011). El consumo de pescado y fauna acuática silvestre en la Amazonía ecuatoriana (1st ed.). Roma: FAO.

Von Bertalanffy, L. (1938). A quantitative theory of organic growth (inquiries on growth laws. II). Human Biology, 10, 181-213.

Wells, R., Kohin, S., Teo, S., Snodgrass, O., & Uosaki, K. (2013). Age and growth, of North Pacific Albacore (Thunnus alalunga): implications for stock assessment. Fisheries Research, 147, 55-62.