PRODUCTION, MODELING, AND EDUCATION. Growth curves for ostriches (Struthio camelus) in a Brazilian population
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1 PRODUCTION, MODELING, AND EDUCATION Growth curves for ostriches (Struthio camelus) in a Brazilian population S. B. Ramos,* S. l. Caetano,* R. P. Savegnago,* B. N. Nunes,* A. A. Ramos, and D. P. munari * 1 * Departamento de Ciências Exatas, Faculdade de Ciências Agrárias e Veterinárias, Universidade Estadual Paulista, , Via de Acesso Prof. Paulo Donato Castellane s/n, Jaboticabal, São Paulo, Brazil; and Departamento de Produção e Exploração Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade Estadual Paulista, , Botucatu, São Paulo, Brazil ABSTRACT The objective of this study was to fit growth curves using nonlinear and linear functions to describe the growth of ostriches in a Brazilian population. The data set consisted of 112 animals with BW measurements from hatching to 383 d of age. Two nonlinear growth functions (Gompertz and logistic) and a third-order polynomial function were applied. The parameters for the models were estimated using the least-squares method and Gauss-Newton algorithm. The goodness-of-fit of the models was assessed using R 2 and the Akaike information criterion. The R 2 calculated for the logistic growth model was for hens and for cockerels and for the Gompertz growth model, for hens and for cockerels. The third-order polynomial fit gave R 2 of for hens and for cockerels. Among the Akaike information criterion calculations, the logistic growth model presented the lowest values in this study, both for hens and for cockerels. Nonlinear models are more appropriate for describing the sigmoid nature of ostrich growth. Key words: growth, nonlinear models, ostrich, Struthio camelus 2013 Poultry Science 92 : INTRODUCTION Growth can be defined as an increase in body size per unit of time (Tompić et al., 2011). modeling growth curves of animals is a necessary tool for optimizing the management and efficiency of animal production (Köhn et al., 2007). However, growth can only be attained under nonlimiting conditions. For example, food needs to be available ad libitum; the nutrient content must at least meet the required ratios in relation to energy; intake must not be constrained by the bulk of the food or the presence of toxins; and environmental factors such as high temperature and disease must not constrain intake (Emmans and Kyriazakis, 1999). An animal s genetic potential for growth can described in terms of its growth curve (Emmans and Fisher, 1986). The available literature on ostrich growth used data from South African farms and modeled only the Gompertz growth function (du Preez et al., 1992; Cilliers et al., 1995; Cooper, 2005). In Brazil, ostrich production began in 1995 with the importation of the first animals from Italy (Carrer et al., 2005). In 2006, the estimated number of commercially farmed birds in the country was 335,425, according to the Brazilian ostrich-rearing Yearbook (Anuário da Estrutiocultura Brasileira, 2013 Poultry Science Association Inc. Received April 3, Accepted September 8, Corresponding author: danisio@fcav.unesp.br 2005/2006). Despite the size of the national flock, no studies describing its growth are available. The objective of this study was to fit growth curves using nonlinear and linear functions to describe the growth of ostriches in the Brazilian population. MATERIALS AND METHODS The data used for the growth analysis came from commercial flocks and were provided by the Brazilian ostrich Rearers Association (Associação dos Criadores de Avestruz do Brasil), based in São Paulo, SP, Brazil. This institute approved the use of this data to perform this research. A total number of 441 BW records from 58 hens and 54 cockerels measured from hatching to 383 d of age were used. The animals were crossbreds from the African Black, Red Neck, and Blue Neck breeds. The exact proportions of these genetic groups within each animal were unknown. Figure 1 shows animals of the African Black breed. Figure 1a shows a triplet consisting of 1 cockerel (at the center) and 2 hens. They are 8-yr-old animals with an approximate BW of 150 kg and approximate height of 2.20 m. Figure 1b shows 8-mo-old male and female chicks, with no visible sexual differentiation in plumage, with approximate BW and height of 75 kg and 1.80 m, respectively. After the chicks had hatched, they were weighed, tagged around the neck for identification, and trans- 277
2 278 Ramos et al. Figure 1. An African Black triplet consisting of one cockerel (at the center) and 2 hens (a); male and female African Black chicks (b). Photos courtesy of Celso da Costa Carrer (Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo). Color version available in the online PDF. ferred to small pens. At night, they were housed in a controlled environment with a minimum temperature of 25 C. When the birds reached 3 mo of age, they were moved to larger pens and were no longer housed. At 6 mo of age, the birds were transferred again to larger pens. The birds diet was composed of pasture grass, specific industrial food with added citric pulp, and water ad libitum.
3 PRODUCTION, MODELING, AND EDUCATION 279 Table 1. Functions for modeling the growth curve and inflection points in the ostrich Model Equation 1 t i 2 y i 3 Reference A Logistic W = ( + Be ( Ct) t ln B A yi 1 C ) = Fekedulegn et al. (1999) 2 Gompertz W = Ae e ( B Ct) B ti = C y A i = Wellock et al. (2004) e Polynomial W = d 0 + d 1 t + d 2 t 2 + d 3 t 3 d t i = 2 y i = 2d 2 Tompić et al. (2011) 3d i = ( ) 1 W = predicted BW (kg) at age t; A = asymptotic final BW (kg); t = age in days; C = instantaneous relative growth rate; B = function-specific parameters; e = base of natural logarithm ( ); d 0 = intercept; and d 1, d 2, and d 3 = regression coefficients. 2 t i = age (d) at inflection point. 3 y i = BW (kg) at inflection point. 3 To estimate the BW at a certain age, two 3-parameter nonlinear growth functions and a polynomial growth function were fitted to the ostrich BW data. The equations for the growth models applied are given in Table 1. The model parameters were estimated and the statistical analysis was carried out using the R software version (R Development Core Team, 2012). The nonlinear and linear modeling was carried out using the NLS and LM procedures, respectively. The LM procedure used the least-squares method and the nonlinear regression the Gauss-Newton algorithm. The initial values for the curve parameters were estimated from earlier reports (du Preez et al., 1992; Cilliers et al., 1995). The goodness-of-fit of the functions was assessed using R 2 and the Akaike information criterion (AIC). The R 2 is defined as the proportion of the total sum of squares that is explained by the model. The range is 0 R 2 1. Values closer to 1 indicate better fit (Faraway, 2004). The AIC is defined as AIC = 2L m + 2m, where L m is the maximized log-likelihood and m is the number of parameters in the model. Lower AIC values indicate the preferred model (Akaike, 1973). The t-test was used to investigate whether the estimates were significantly different from zero and to compare nonlinear model parameter estimates for cockerels and hens. The inflection points of the nonlinear functions and the third-order polynomial were calculated. The equations for calculating the inflection points of these functions are given in Table 1. RESULTS Table 2 shows the estimated fitting parameters, their SE, R 2, AIC, and inflection points of the Gompertz and logistic functions. Parameter A of the nonlinear growth curves, which can be interpreted as the asymptotic final BW, was greater in the Gompertz function than in the logistic function, both for cockerels and for hens (P < 0.05). Parameter C, which can be interpreted as the instantaneous relative growth rate, was also greater in the logistic function than in the Gompertz function, both for cockerels and for hens (P < 0.05). There were no significant differences in mature weights and instantaneous relative growth rates between cockerels and hens, for either of the nonlinear growth functions. The logistic curve showed higher R 2 values both for hens and for cockerels. According to the nonlinear functions, the hens reached the inflection point at an earlier age than the cockerels. However, the third-order polynomial function showed the opposite. Both of the nonlinear functions showed that the cockerels had greater BW at the inflection point. Table 3 shows the estimated fitting parameters, their SE, R 2, AIC, and inflection points of the third-order polynomial fit. The intercept (d 0 ) can be interpreted as the mean BW at hatching. The estimate of d 0 was negative but not significantly different from zero. The Table 2. Estimated parameters, SE, inflection point, R 2, and Akaike information criterion (AIC) for 2 nonlinear growth curves Model parameter 1,2 Point of inflection 3 Model Sex A B C t i y i R 2 AIC Logistic Female (2.124) a (4.269) (0.001) a ,576 Male (2.815) a (3.860) (0.001) a ,560 Gompertz Female (5.441) b 1.55 (0.063) (0.001) b ,605 Male (7.174) b (0.066) (0.001) b ,571 a,b Means within a column with different superscripts differ significantly (P < 0.05). 1 A = asymptotic final BW (kg); B = function-specific parameter; C = instantaneous relative growth rate. 2 Standard errors are between parentheses. 3 t i = age (d) at point of inflection; y i = BW (kg) at point of inflection.
4 280 Ramos et al. Table 3. Estimated parameters, SE, inflection point, R 2, and Akaike information criterion (AIC) for third-order polynomial growth model Model parameter 1,2 Point of inflection 3 Sex d 0 d 1 d 2 d 3 t i y i R 2 AIC Female (1.049) (0.030) (0.300) (0.500) ,598 Male (1.255) (0.038) (0.300) (0.600) ,568 1 d 0 = intercept; d 1 = regression coefficient; d 2 = regression coefficient ( 10 3 ); d 3 = regression coefficient ( 10 6 ). 2 Standard errors are shown between parentheses. 3 t i = age (d 10 9 ) at point of inflection; y i = BW (kg) at point of inflection. estimate of the regression coefficient of the first power term (d 1 ) was also not significantly different from zero. Among the polynomial and nonlinear functions, the logistic curve showed the highest R 2 and lowest AIC values, both for hens and for cockerels. Except for the third-order polynomial parameters with estimates not significantly different from zero, all the models showed small SE, thus indicating accurate estimates of the parameters. Figures 2 and 3 show the results from all the models applied to the hens and cockerels, respectively. Visually, all 3 growth models showed similar fits from the start to the end of the growth period. The third-order polynomial showed a slightly decrease in BW at the end of the growth period. The Gompertz model suggested that growth had not stopped at the end of the period. The logistic model showed the best fit of all the models. DISCUSSION Growth is an important attribute of organisms and the efforts to predict it that have been made can be seen in the large number of functions that have been Figure 2. Growth curves of females. Observed data are shown as circles; lines are modeled curves using the estimated parameters of each of the following functions: (a) logistic, (b) Gompertz, and (c) third-order polynomial. y = predicted BW (kg) at age t (d).
5 PRODUCTION, MODELING, AND EDUCATION 281 Figure 3. Growth curves of males. Observed data are shown as circles; lines are modeled curves using the estimated parameters of each of the following functions: (a) logistic, (b) Gompertz, and (c) third-order polynomial. y = predicted BW (kg) at age t (d). created (Fekedulegn et al., 1999; Wellock et al., 2004). Among the nonlinear functions, the logistic and Gompertz functions were chosen for this study because of their economy of parameters and ability to describe relative growth rate as a simple function of size. They can also describe continuous growth, sigmoid forms, asymptotes, inflection points, and parameters with biological interpretations. All these properties are desirable in nonlinear growth models (Wellock et al., 2004). The third-order polynomial was chosen because of its resemblance to nonlinear growth functions. The R 2 values calculated for all the models were very similar, but the logistic growth function showed a slightly higher value. The logistic growth function also showed the smallest calculated AIC value. The R 2 measures linear associations and is therefore a goodnessof-fit measurement that is more appropriate for linear models. The AIC is a more appropriate goodness-of-fit measurement for use in comparisons between linear and nonlinear models and functions with different numbers of parameters. The estimates for the parameters A and C, which can be interpreted as mature BW and instantaneous relative growth rate, respectively, were similar to those found in previous studies on ostrich growth. du Preez et al. (1992) found mature BW estimates of ± 3.72 kg for cockerels and 98.4 ± 4.2 kg for hens and instantaneous relative growth rate estimates of 9.7 ± 0.43 ( 10 3 ) for cockerels and 9.0 ± 0.44 ( 10 3 ) for hens. Cilliers et al. (1995) found mature BW estimates of ± 2.48 kg for cockerels and ± 3.47 kg for hens and instantaneous relative growth rate estimates of 9.10 ± 0.28 ( 10 3 ) for cockerels and 8.50 ± 0.41 ( 10 3 ) for hens. The values for inflection points relating to age that were found in this study (Tables 2 and 3) were also similar to what has been reported in the literature. du Preez et al. (1992) found an inflection point for age, which was interpreted as the age at maximum weight gain, of 163 d for cockerels and 175 d for hens. Cilliers et al. (1995) found inflection points for age of d for cockerels and d for hens. The Gompertz model suggested that growth had not stopped at the end of the period. This may be an indication that the birds in this study were not fully matured at the end of the period.
6 282 Ramos et al. According to R 2 and the AIC, the third-order polynomial showed a good fit. Tompić et al. (2011) found a similar result. Compared with the nonlinear models, linear models lack parameters with biological interpretation, but such models can be linearized and their parameters estimated by means of linear regression. Further studies are needed to understand ostrich growth in Brazil. Ideally, study data sets should contain a large number of birds, each with the same number of BW records, collected at regular intervals that are not too close, so that the measurements are neither correlated nor too distant, such that there are not enough classes. The present study suggests that the logistic model is appropriate for describing ostrich growth, both for cockerels and for hens. ACKNOWLEDGMENTS We thank ACAB (Associação dos Criadores de Avestruzes do Brasil, São Paulo, SP, Brazil) for the data set and Celso da Costa Carrer, from Faculdade de Zootecnia e Engenharia de Alimentos, Universidade de São Paulo, for photos. Financial support was provided by FAPESP (Fundação de Amparo a Pesquisa do Estado de São Paulo, Brazil), CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brasília, DF, Brazil), and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brasília, DF, Brazil). S. B. Ramos and B. N. Nunes were granted scholarships from CAPES Programa de Pós-graduação em Genética e Melhoramento Animal, Curso Doutorado, FCAV/UNESP. S. B. Ramos, R. P. Savegnago, and S. L. Caetano received scholarships from FAPESP. D. P. Munari was the recipient of a fellowship from CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico). REFERENCES Akaike, H Information theory and an extension of the maximum likelihood principle. Pages in 2nd Int. Symp. Inf. Theory, Budapest, Hungary. Tsahkadsor, Armenian SSR. Anuário da Estrutiocultura Brasileira. 2005/2006. Ed. Associação dos Criadores de Avestruzes do Brasil, São Paulo, Brazil. Carrer, C. C., R. A. Elmôr, and R. D. Rosa Manual do Programa de Melhoramento Genético do Avestruz Brasileiro. Associação dos Criadores de Avestruzes do Brasil/Programa de Melhoramento Genético do Avestruz Brasileiro, São Paulo, Brazil. Cilliers, S. C., J. J. du Preez, J. S. Maritz, and J. P. Hayes Growth curves of ostriches (Struthio camelus) from Oudtshoorn in South Africa. Anim. Sci. 61: Cooper, R. G Growth in the ostrich (Struthio camelus var. domesticus). Anim. Sci. J. 76:1 4. du Preez, J. J., M. J. F. Jarvis, D. Capatos, and J. de Kock A note on growth curves for the ostrich (Struthio camelus). Anim. Prod. 54: Emmans, G. C., and C. Fisher Problems in nutritional theory. Proc. Br. Poult. Sci. Symp Emmans, G. C., and I. Kyriazakis Growth and body composition. Pages in A Quantitative Biology of the Pig. I. Kyriazakis, ed. CAB Int., Wallingford, UK. Faraway, J. J Linear Models with R. 1st ed. Chapman and Hall/CRC, Boca Raton, FL. Fekedulegn, D., M. Mac Siurtain, and J. Colbert Parameter estimation of nonlinear growth models in forestry. Silva Fennica 33: Köhn, F., A. R. Sharifi, and H. Simianer Modeling the growth of the Goettingen minipig. J. Anim. Sci. 85: R Development Core Team R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Tompić, T., J. Dobša, S. Legen, N. Tompić, and H. Medić Modeling the growth pattern of in-season and off-season Ross 308 broiler breeder flocks. Poult. Sci. 90: Wellock, I. J., G. C. Emmans, and I. Kyriazakis Describing and predicting potential growth in the pig. Anim. Sci. 78:
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