Aquaculture 511 (2019) 734243

Contents lists available at ScienceDirect

Aquaculture
journal homepage: www.elsevier.com/locate/aquaculture

Growth curves by Gompertz nonlinear regression model for male and female T
Nile tilapias from different genetic groups
⁎
Aline Mayra da Silva Oliveira Zardina, , Carlos Antonio Lopes de Oliveiraa,b,
Sheila Nogueira de Oliveirab,c, Grazyella Massako Yoshidab, Danusia Tavares de Albuquerquec,
Cristiane Meldau de Camposa, Ricardo Pereira Ribeirob
a
Programa de Pós-Graduação em Zootecnia, Produção Animal do Cerrado-Pantanal, Universidade Estadual de Mato Grosso do Sul, Rod. Aquidauana/UEMS km 12, C.P.
25, 79200-000 Aquidauana, MS, Brazil
b
Grupo de Pesquisa Peixegen, Universidade Estadual de Maringá, Av. Colombo 5790, Jardim Universitário, 87020-900 Maringá, PR, Brazil
c
Universidade Federal da Grande Dourados, Faculdade de Ciências Agrárias, Rodovia Dourados/Itahum, Km 12 - Unidade II, 79, 804-970 Dourados, MS, Brazil

A R T I C LE I N FO A B S T R A C T

Keywords: The aim of this study was to estimate the growth curve of Nile tilapia from different genetic groups and to
Breeding program examine possible differences in the growth between sexes using the Gompertz model. The Gompertz function
Breeding value was tested with eight different models: the first model without restriction in the parametric space and the other
Growth model models at were restricted one, two or three parameters. The fish were classified into three genetic groups:
Growth rate
Superior, Medium, and Inferior according to their estimated breeding value for average daily weight gain.
Oreochromis niloticus
Weight
Growth of genetic groups indicated that male and female fish showed similar growth during the first 165 days of
age, probably due to the onset of reproduction. The estimated asymptotic values for body weight of males from
Medium and Inferior group were 69% and 49% smaller than the asymptotic weight of Superior males, respec-
tively, confirming the impact of genetic differences on the phenotypic expression in fish, in which animals with
high estimated breeding value (Superior group) had a higher growth rate than others. The Gompertz model was
useful to describe growth in Nile tilapias. The estimates of asymptotic weight for females were smaller than of
males. Fish from the Superior genetic group presented higher growth rate, asymptotic weight than other groups
in both sexes.

1. Introduction Studies of growth curves in tilapias by using equations that can

Tilapia farming is growing in many parts of the world and Brazil is
the fourth largest producer of this species, with a production of 357,639
tons in 2017, corresponding to 51.7% of the total Fish farm production
in Brazil (PeixeBR, 2018). Growth in world-wide tilapia culture and the
continuous intensification of the culture systems has resulted in a
constant search for strains with superior growth performance (Costa
et al., 2009; Lago et al., 2017).
predict the animal's weight based on its age have been very useful, as
they summarize information from a data series into a small set of bio-
logically interpretable parameters (Santos et al., 2007). According to
Fitzhugh Jr. (1976), the growth curve is sigmoidal in shape, which
represents the behavior of body weight, length or height in relation to
the animal's age. Growth during the first stage of life is slow, followed
by a period of auto-acceleration, until the point of maximum growth
rate is reached, close to puberty, when an auto-slowdown phase occurs

Abbreviations: EBV, Estimated breeding value; C1, Contrast one - Superior males versus Superior females; C2, Contrast two - Medium males versus Medium females;
C3, Contrast three - Inferior males versus Inferior females; C4, Contrast four - Superior males versus Medium males; C5, Contrast five - Superior males versus Inferior
males; C6, Contrast six - Medium males versus Inferior males; C7, Contrast seven - Superior females versus Medium females; C8, Contrast eight - Superior females
versus Inferior females; C9, Contrast nine - Medium females versus Inferior females; M1, Model one, did not present restriction in the parametric space; M2, M3, and
M4, Models two, three and four. These three models present restriction of one parameter of the growth function; M5, M6 and M7, Models five, six and seven. These
three models present restriction of two parameters of the growth function;M8, Model eight, with restriction of three parameters of the growth function; RSS, Residual
sum of squares.
⁎
Corresponding author.
E-mail addresses: amsozoo@gmail.com (A.M.d.S. Oliveira Zardin), caloliveira@uem.br (C.A.L. de Oliveira), sheilanoliveira@ufgd.edu.br (S.N. de Oliveira),
cmeldau@uems.br (C.M. de Campos), rpribeiro@uem.br (R.P. Ribeiro).

https://doi.org/10.1016/j.aquaculture.2019.734243
Received 22 June 2018; Received in revised form 28 May 2019
Available online 24 June 2019
0044-8486/ © 2019 Elsevier B.V. All rights reserved.
A.M.d.S. Oliveira Zardin, et al. Aquaculture 511 (2019) 734243

Table 1 Gompertz and Richards). However, the Gompertz and Von Bertalanffy
Description of the tested models. models were the best fit for Chitralada and Supreme tilapia strains. In
Models adjustments growth study of Nile tilapia in the Sub middle of the São Francisco
River, Sousa Jr et al. (2014), testing these same models, found that the
M 1 M 2 M 3 M 4 M 5 M 6 M 7 M 8 models of better fit to the data were Bertalanffy, Logistic and Gompertz.
Furthermore, these models were recommended to monitor weight gain
Parameters ai ai ai A* ai A* A* A*
bi bi B* bi B* B* bi B* of tilapia with crops up to 270 days reared in net cages.
ci C* ci ci C* ci C* C* According to Fialho (1999), the Gompertz model is advantageous to
aj aj aj A* aj A* A* A* adjust growth curves because, unlike other functions, the initial body
bj bj B* bj B* B* bj B* mass is always greater than zero. The Gompertz model is suitable do
cj C* cj cj C* cj C* C*
describe the earlier growth in fish (Gamito,1998), and can be produce
Parameters a, b and c are from the Gompertz model where i and j identified the better fit when the growth rate of fish changes throughout the growth
sexes and genetic groups; * the capital letter indicated the same parameter. period until adult stage, as described by Santos et al. (2013).
When evaluating the body growth of Genetically Improved Farmed
(Berg and Butterfield, 1976). Tilapia (GIFT) tilapia strain using different mathematical models,
Nonlinear functions used to model the age–weight relation to de- Amancio et al. (2014) suggested the use of Gompertz model for de-
scribe the growth curve, traditionally including Brody, Richards, Von scribing the body-growth curve because it presents the best fit for the
Bertalanffy, Gompertz, and Logistic growth functions (Mazzini et al., data and more accurately estimating biological parameters.
2003; Santos et al., 2007; Costa et al., 2009; Loaiza-Echeverri et al., Understanding body growth is important for animal breeding. In
2013; Oliveira et al., 2013; Amancio et al., 2014). Nonlinear equations tilapia breeding programs, the growth rate is often chosen as a selection
present different biological interpretation meaning related to initial criterion because it is related to the body shape and morphometric
conditions, growth rate, or adult body weight, all linked to economic measurements of the animal (Huang and Liao, 1990). The growth rate
aspects of production (Mello et al., 2015). And those were used in many can be predicted by the growth mathematical functions and the same
studies of many fish species like Dourada (Gamito, 1998), Atlantic blue functions can estimate changes in curves form during the animal se-
marlin, Blacktip shark, Tautog, Atlantic spadefish, Yellowtail, Redear lection based on important economic characteristics, and yet predict or
sunfish (Hernandez-Llamas and Ratkowsky, 2004); Piracanjuba adjust the ideal age for slaughtering (Knizetova et al., 1991). According
(Gomiero et al., 2009); and Tambaqui (Mello et al., 2015). to Ibáñez-Escriche and Blasco (2011), the knowledge about the speed of
The application of nonlinear models for the adjustment of growth growth of different tissues has high value to the meat production in-
curves of the Nile tilapia, as reported by Santos et al. (2007), was sa- dustry.
tisfactory for all the tested models (Brody, Von Bertalanffy, Logistic, The existence of different growth curves in relation to the fish

Table 2
Estimates of the unrestricted and restricted models' parameters, adjusted for weight of males versus females of Superior (C1), Medium (C2) and Inferior (C3) groups
and respective residual sum of squares (RSS).
Parameters Models parameters estimates

M1 M2 M3 M4 M5 M6 M7 M8

Contrast 1 (C1)

ai 1,100 1,064 1,089 1,000 1,056 2,836 53,196 813

bi 0.00688 0.00702 0.00692 0.00731 0.00692 0.00401 0.00188 0.00724
ci 308 303 307 295 303 474 1151 292
aj 660 710 672 – 716 – – –
bj 0.00701 0.00666 – 0.00544 – – 0.00196 –
cj 293 – 295 356 – 514 – –
RSS 2,495,756 2,496,042 2,495,777 2,500,843 2,505,300* 2,644,508 2,714,593 4,632,857

Contrast 2 (C2)

ai 743 706 725 677 704 1,403 16,247 617

bi 0.00697 0.00723 0.0071 0.00746 0.00706 0.00447 0.00207 0.00698
ci 282 274 278 269 275 394 947 276
aj 433 497 457 – 502 – – –
bj 0.00741 0.00667 – 0.00544 – – 0.00217 –
cj 254 – 262 324 – 430 – –
RSS 9,902,807 9,906,178 9,903,439* 9,924,133 9,953,389 10,347,742 10,589,231 13,797,610

Contrast 3 (C3)

ai 519 524 532 506 522 675 3,115 462

bi 0.00703 0.00698 0.0069 0.00715 0.0069 0.00562 0.00291 0.00708
ci 269 270 273 266 270 312 625 264
aj 415 395 371 – 398 – – –
bj 0.00634 0.00657 – 0.00556 – – 0.00313 –
cj 278 – 261 310 – 342 – –
RSS 2,084,806 2,084,835 2,084,976 2,085,112 2,087,507* 2,116,675 2,154,676 2,357,112

The parameters a, b and c are from Gompertz model where i = males and j = females. In C1 i = males Superior versus j = females Superior; C2 i = males Medium
versus j = females Medium; C3 i = males Inferior versus j = females Inferior. - indicates equality of parameters. *Best fit model for the χ2 (P < .05) statistic.

2
A.M.d.S. Oliveira Zardin, et al. Aquaculture 511 (2019) 734243

Table 3
Estimates of the unrestricted and restricted models' parameters, adjusted for weight between males of the Superior versus Medium (C4), Superior versus Inferior (C5),
Medium versus Inferior (C6) group and respective residual sum of squares (RSS).
Parameters Models parameters estimates

M1 M2 M3 M4 M5 M6 M7 M8

Contrast 4 (C4)

ai 1,100 962 1,082 856 989 1,268 4,080 1,009

bi 0.00688 0.00752 0.00695 0.00817 0.00669 0.00535 0.00319 0.00612
ci 308 290 306 275 296 341 576 319
aj 743 786 747 – 830 – – –
bj 0.00697 0.00671 – 0.00635 – – 0.00335 –
cj 282 – 282 302 – 360 – –
RSS 8,282,534 8,284,869 8,282,560* 8,293,443 8,376,483 8,560,859 8,744,236 9,190,111

Contrast 5 (C5)

ai 1,100 1,025 1,087 977 1,179 11,490 376 9,109

bi 0.00688 0.0072 0.00693 0.00743 0.0062 0.00256 0.0241 0.00287
ci 308 298 306 292 321 780 208 717
aj 519 631 529 – 771 – – –
bj 0.00703 0.00615 – 0.00482 – – 0.00875 –
cj 269 – 272 371 – 820 – –
RSS 3,286,535 3,288,409 3,286,564* 3,297,419 3,368,788 3,536,015 4,488,771 5,538,646

Contrast 6 (C6)

ai 743 735 742 721 741 903 390 801

bi 0.00697 0.00703 0.00698 0.00712 0.00693 0.00596 0.0129 0.00642
ci 282 280 281 277 281 312 209 299
aj 519 560 523 – 573 – – –
bj 0.00703 0.00666 – 0.00568 – – 0.00848 –
cj 269 – 270 319 – 339 – –
RSS 8,511,195 8,511,492 8,511,200 8,515,047 8,522,034* 8,632,773 9,473,587 9,589,535

The parameters a, b and c are from Gompertz model. In C4 i = Superior versus j = Medium; C5 i = Superior versus j = Inferior; C6 i = Medium versus j = Inferior. -
indicates equality of parameters. *Best fit model for the χ2 (P < .05) statistic.

genetic groups can be an indicator of the results from the breeding
program. This study aimed at improving our understanding of growth
curves and to evaluate the results from the genetic breeding program
for the Nile tilapia in Brazil. In order to estimate the growth curves for
male and female tilapias by the nonlinear Gompertz model and examine
possible differences in the growth between sexes the fish were classified
into different genetic groups.
2. Materials and methods
performed according the manufacture's specifications, considering the
total biomass at the cages, it ranged from 10% to 2% of total biomass.
The body weight was obtained every 30 day using an electronic
scale (Toledo, model 9094, 6 kg). To reduce the stress during the ma-
nipulation to collect the weight, we used 25 mg eugenol for each liter of
water, according Vidal et al. (2008), 75 mg/L is recommend to produce
a fast and deep anesthesia. The water temperature and dissolved
oxygen, ranged from 19 to 26 °C and from 3.8 to 6.8 mg/L (Oliveira
et al., 2016).

2.1. Data set 2.2. Genetic groups

The dataset contained information from 1719 fish that were off-
spring of 58 full-sib and half-sib families from the genetic improvement
program for a GIFT strain obtained from the State University of
Maringá, UEM. The animals were reared at Fish Farming Experimental
Station of the UEM/Codapar, in Floriano, PR (23° 31′ 8″ S 52° 2′ 21″ W)
between November 2008 and February 2009. After reaching an average
body weight of about 10 g, the fish were tagged with a microchip im-
planted in the visceral cavity. Then, biometric measurements of the
tagged fish were performed and the fish sent to the UEM production
unit, Diamante do Norte, PR (22° 39′ 24″ S 52° 46′ 51″ W), in the Corvo
River, a tributary of the Paranapanema River in the Rosana reservoir.
The male and female fish were cultivated in three cages
(2 × 2 × 1.5 m), the stocking density was 100 fish per m3. The per-
formance test was conducted from May to September 2009. In the first
30 days, the diet was commercial dry pellet feed with 45% crude pro-
tein provided to the fish three times a day; thereafter, the dry pellets
with 32% crude protein were provided twice a day until harvest, as
described by Oliveira et al. (2016), and the feeding adjustment was
Fish were segregated into three genetic groups, using as criterion
the estimated breeding value, EBV (high, medium and low EBV) for
daily weight gain. The breeding values were estimated using the animal
model, according the Henderson's mixed-model equations (Henderson,
1984) as described by Oliveira et al. (2014).
The genetic groups were, Superior (the EBV ranged from 0.615 to
0.216) consisted of 142 males and 142 females, the Medium Group
where the EBV ranged from 0.215 to 0.014 and the number of males
and female were 645 and 528 respectively, and the Inferior with 184
males and 77 females had the EBV ranged from 0.013 to −0.248.
The comparisons of fish growth standard were made between sexes
within each genetic group, generating the following contrasts:
C1 = Superior males versus Superior females; C2 = Medium males
versus Medium females; C3 = Inferior males versus Inferior females. The
contrasts among the genetic groups within sex were, C4 = Superior
males versus Medium males; C5 = Superior males versus Inferior males;
C6 = Medium males versus Inferior males; C7 = Superior females versus
Medium females; C8 = Superior females versus Inferior females; and

3
A.M.d.S. Oliveira Zardin, et al. Aquaculture 511 (2019) 734243

Table 4
Estimates of the unrestricted and restricted models' parameters, adjusted for weight between females of Superior versus Medium (C7), Superior versus Inferior (C8),
Medium versus Inferior (C9) group and respective residual sum of squares (RSS).
Parameters Models parameters estimates

M1 M2 M3 M4 M5 M6 M7 M8

Contrast 7 (C7)

ai 660 549 623 508 577 698 1,776 597

bi 0.00701 0.00803 0.0073 0.00855 0.00688 0.00569 0.00351 0.00632
ci 293 268 285 258 276 310 496 295
aj 433 475 441 – 506 – – –
bj 0.00741 0.00689 – 0.00656 – – 0.00368 –
cj 254 – 257 278 – 324 – –
RSS 4,116,029 4,119,097 4,116,231* 4,123,530 4,178,233 4,250,880 4,330,011 4,394,257

Contrast 8 (C8)

ai 660 651 678 633 727 1,859 18,630 1,473

bi 0.00701 0.00707 0.00687 0.00721 0.00632 0.00386 0.00202 0.00436
ci 292 291 297 287 308 478 1021 437
aj 415 450 373 – 529 – – –
bj 0.00634 0.006 – 0.00489 – – 0.0021 –
cj 278 – 262 350 – 509 – –
RSS 1,294,027* 1,294,086* 1,294,185* 1,295,077* 1,317,586 1,362,519 1,384,547 1,703,857

Contrast 9 (C9)

ai 433 438 440 432 439 468 960 444

bi 0.00741 0.00735 0.00732 0.00743 0.0073 0.00686 0.0044 0.00713
ci 254 256 257 254 256 266 391 261
aj 415 358 345 – 361 – – –
bj 0.00634 0.00707 – 0.00616 – – 0.00496 –
cj 278 – 250 285 – 288 – –
RSS 3,476,417 3,476,677 3,476,880 3,476,432 3,477,808* 3,497,162 3,563,819 3,644,538

The parameters a, b and c are from Gompertz model. In C7 i = Superior versus j = Medium; C8 i = Superior versus j = Inferior; C9 i = Medium versus j = Inferior. -
indicates equality of parameters. *Best fit model for the χ2 (P < .05) statistic.

C9 = Medium females versus Inferior females. 3. Results and discussion

The corporal weight data adjusted properly to the Gompertz model,

2.3. Statistical analysis
all tested models reached the convergence. In the models M6 and M7,
the asymptotic weight (parameter a) and the age at the inflection point
To describe the fish growth, the Gompertz nonlinear regression
(parameter c) were overestimated comparing to the others models
model (Fialho, 1999) was adjusted to body weight data as follows:
(Table 2). This was also observed when comparing the growth curves
M = A exp− exp
−B (t − C)
(1) between the genetic groups with fishes of same sex in models M6 (C5,
C6 and C8), M7 (C4, C7, C8 and C9) and M8 (C5 and C8) (Tables 3 and
where M = weight (g) estimate at age t; A = asymptotic weight (g) 4).
when t tends to infinity it can be interpreted as weight to adult age; According to our results, the best adjustments were observed in
B = relative growth at the inflection point (g/day per gram); C = age at models with different parameters to males and females within the same
the inflection point (days); t = age (days); exp = 2.718281828459. genetic group (Table 3). Thus the male and female growth patterns
To determine the growth rate (g/day), the following equation de- were different.
rived from Eq. (1) was used as suggested by Fialho (1999): The best models were those determined different asymptotic
−B (t − C)
weights, M5 to Superior and Inferior genetic group and M3 Medium
dM/dt = ABexp−B(t − C) − exp (2) genetic groups. The males' asymptotic weight was bigger than females
(Table 2). Besides the differences in the asymptotic weights (parameter
A total of eight models were tested for each contrast, the first model
a), the relative growth (parameter b) and the inflection point (para-
(M1) did not present restriction in the parametric space, such that all
meter c) were equal for both sexes in the Superior and Inferior genetic
the Gompertz curve parameters were different between sexes or groups.
groups. In Medium group, the inflection points estimates were different
At other models were restricted one, two or three parameters of the
between males and females (Table 2).
growth functions. A detailed description of the growth curve para-
Although both sexes presented the same relative growth, the males
meters omitted in different growth models is given in Table 1.
maintained the growth for an additional 16 days (Fig. 1, C2-a and C2-
The growth curve parameters were estimated using the Gauss
b). According to Mello et al. (2015), from growth curves by Gompertz
Newton method modified, the analysis were performed using the NLIN
model it is possible to estimate the maximum growth rate and, thus, fit
procedure in the SAS system version 9 (SAS Institute Inc., 2002). To
the better slaughter age for each sex.
select the model that best describes the growth curve the likelihood
In the different genetic groups estimates, the males showed higher
ratio test was applied for equality of parameters of non-linear models,
values for weight at maturity than females. This phenomenon could be
with approximation to the chi-square statistic (χ2) described as by
associated with sexual dimorphism reported as reported earlier in Nile
Regazzi and Silva (2004).

4
A.M.d.S. Oliveira Zardin, et al.
Fig. 1. Adjusted growth curves (a) in relation to the age and growth rate (b) of males versus females of the Superior (C1), Medium (C2) and Inferior (C3) groups of
Nile tilapias Genetic improvement program at the State University of Maringá.
tilapias (Oliveira et al., 2013; Lind et al., 2015; Lago et al., 2017). The
standard weight increment measurements of the three genetic groups
indicated that males and females of each group showed similar growth
for approximately 165 days of life, after that the females presented
slower growth. Probably this is due to the onset of reproduction
(Fig. 1), where the energy used for corporeal growth is redirected to the
gonadal development as suggested by Baldisserotto (2009).
According to the results obtained, it can be seen that in short-cycle
cultivation, when the objective is to have a lower slaughter weight
(< 700 g) in cages, the animals in this breeding program can be used
without sexual inversion, reducing costs and optimizing the production
process. According to Kamaruzzaman et al. (2009) monosex production
in tilapia may be more beneficial in slow-growing strains that fre-
quently reach early sexual maturity, leading to breeding and over-
crowding in ponds.
In assessing the growth curves of males and females in tilapias from
the different genetic groups, Lago et al. (2017) observed differences in
growth patterns between males and females, with higher weight and
specific growth rate to males. However, Rutten et al. (2005) verified
that the female growth curves increased linearly and did not stabilize
after the inflection point (sexual maturity), suggesting that ambient
conditions (high stocking density) were the reason for females to
5
Aquaculture 511 (2019) 734243
continue growing.
The growth curves for males between genetic groups (contrasts C4,
C5), indicated that the best model was M3. There was observed dif-
ferences between the asymptotic weights and age at the inflection
point. The estimated asymptotic weights were 1.082, 747 and 529 g for
Superior, Medium and Inferior genetic groups.
The males from Superior genetic group kept the growth rate for 24
and 35 days more than the males of the Medium and Inferior genetic
groups (Table 3). The maximum estimated growth rates were 2.8, 1.9,
and 1.4 g/day for fish of the Superior, Medium, and Inferior group,
respectively (Fig. 2).
The growth curve for the males in C4 and C5 were similar for ap-
proximately 225 and 180 days of life, respectively. However, after the
inflection point, there was an increase in the difference in weight, due
the growth rate of the Superior genetic group (2.8 g/day) (Fig. 2, C4-a
and C4-b; C5-a and C5-b).
The estimates of males from Medium and Inferior genetic groups
were 69% and 49%, respectively, presenting lower values than the es-
timates of the Superior genetic group, pointing the impact of the genetic
difference in the phenotypic expression between genetic groups, in
which animals with high EBV (Superior group) had a higher growth
rate than others (Table 3).
A.M.d.S. Oliveira Zardin, et al.
Fig. 2. Comparison of the adjusted weight growth curves (a) in relation to the age and growth rate (b) between males of Superior versus Medium (C4), Superior versus
Inferior (C5), Medium versus Inferior (C6) groups of Nile tilapias from genetic improvement program at the State University of Maringá.
The growth curves of the Superior versus Medium females (C7) were
similar to that described for males, where the model M3 was the most
appropriate (Table 4). Females from the Superior genetic group pre-
sented higher asymptotic weight and age at the inflection point than
those from the Medium group. The females from Superior genetic group
kept their growth for 29 days more than females from Medium group,
indicating a possible late sexual maturity. Additionally the maximum
growth rates found in both genetic groups were 1.7 and 1.2 g/day for
Superior and Medium females, respectively (Table 4; Fig. 3, C7-a and
C7-b).
Related the growth of Superior and Inferior females (C8), four
models (M1, M2, M3 and M4) may be considered adequate. These
findings are supported by Regazzi and Silva (2004), the information
criterion Akaike (AIC) was used as an additional option, the results
pointed out the best model was the model M2, where the asymptotic
weight and relative growth at the inflection point were different be-
tween the groups. The maximum growth rates were 1.7 and 1.0 g/day
for Superior and Inferior females, respectively, indicating higher weight
until maturity and higher growth rates for the female of Superior ge-
netic group(Fig. 3, C8-a and C8-b).
The relative growth and age to maturity were similar for Medium
6
Aquaculture 511 (2019) 734243
versus Inferior females (C9), however the Medium females presented
higher asymptotic weight than female from Inferior genetic group. The
maximum growth rates for the Medium and Inferior females were 1.2
and 1.0 g/day, respectively.
The growth parameters in fish differ between species, possibly even
within the same species and between sexes (Sparre and Venema, 1998).
Our results showed differences in growth curve parameters between
males and females within of same genetic groups and between the ge-
netic groups for each sex.
4. Conclusions
The Gompertz model was useful to describe the growth pattern in
Nile tilapia, presenting different parameters for males and females and
for each genetic group proposed.
The selection to growth rate did not reduce the dimorphism sexual
in Nile tilapia, because, regardless of the genetic group, the females
presented lower asymptotic weight than males.
Fish from the Superior genetic group had a higher growth rate and
asymptotic weight than the other groups in both sexes.
A.M.d.S. Oliveira Zardin, et al.
Fig. 3. Comparison of adjusted weight growth curves (a) in relation to the age and growth rate (b) between females of Superior versus Medium (C7), Superior versus
Inferior (C8), Medium versus Inferior (C9) groups of Nile tilapias from genetic improvement program at the State University of Maringá.
Acknowledgments
The authors acknowledge the National Scientific and Technological
Development Council-CNPq (471654/2009-4) for granting of financial
support. We thank Peixegen Research Group for kindly providing the
data set. The authors would like to thank Renan da Silva Dalago who
help us at final edition. This work was developed as part of the re-
quirements for the Master dissertation of A.M.S. Oliveira Zardin in
Animal Production on Cerrado-Pantanal at State University of Mato
Grosso of Sul (UEMS).
Declaration of Competing Interests
Authors declare that they don't have any conflict of interest.
Contributors
Zardin A.M.S.·O. and Oliveira C.A.L. participated in the research,
performed the statistical analyses, interpretation of data and drafted the
manuscript.
7
Aquaculture 511 (2019) 734243
Oliveira C.A.L. and Ribeiro.P.R. supervised the research and con-
tributed to manuscript preparation.
Yoshida G.M. and Oliveira S.N. performed the experiment, acqui-
sition of data and manuscript preparation.
Albuquerque D. T. and Campos C. F.M. contributed to manuscript
preparation.
References
Fitzhugh Jr., H.A., 1976. Analysis of growth curves and strategies for altering their shape.
J. Anim. Sci. 42, 1036–1051. https://doi.org/10.2527/jas1976.4241036x.
Amancio, A.L.L., Silva, J.H.V., Fernandes, J.B.K., Sakomura, N.K., Cruz, G.R.B., 2014. Use
of mathematical models in the study of bodily growth in GIFT strain Nile tilapia. Rev.
Ciênc. Agron. 45, 257–266. https://doi.org/10.1590/S1806-66902014000200005.
Baldisserotto, B., 2009. Fisiologia de Peixes Aplicada à Piscicultura, second ed.
Universidade Federal de Santa Maria, Santa Maria.
Berg, R.T., Butterfield, R.M., 1976. New Concepts of Cattle Growth. Sydney University
Press, Sydney.
Costa, A.C., Reis Neto, R.V., Freitas, R.T.F., Freato, T.A., Lago, A.A., Santos, V.B., 2009.
Avaliação do crescimento de tilápias de diferentes linhagens através dos modelos não
lineares. Arch. Zootec. 58 (Supl. 1), 561–564. http://www.uco.es/organiza/
servicios/publica/az/php/img/web/19_13_18_20AvaliacaoCosta.pdf.
Fialho, F.B., 1999. Interpretação da Curva de Crescimento de Gompertz. Embrapa Suínos
A.M.d.S. Oliveira Zardin, et al.
e Aves, Concórdia. Comunicado Técnico. 237.
Gamito, S., 1998. Growth models and their use in ecological modelling: an application to
a fish population. Ecol. Model. 113, 83–94. https://doi.org/10.1016/S0304-
3800(98)00136-7.
Gomiero, J.S.G., Freitas, R.T.F., Santos, V.B., Silva, F.F., Rodrigues, P.B., Logato, P.V.R.,
2009. Curvas de crescimento morfométrico de Piracanjuba (Brycon orbignyanus).
Ciênc. Agrotec. 33, 882–889. https://doi.org/10.1590/S1413-70542009000300031.
Henderson, C.R., 1984. Applications of Linear Models in Animal Breeding. University of
Guelph, Guelph.
Hernandez-Llamas, A., Ratkowsky, D.A., 2004. Growth of fishes, crustaceans and mol-
luscs: estimation of the von Bertalanffy, Logistic, Gompertz and Richards curves and a
new growth model. Mar. Ecol. Prog. Ser. 282, 237–244. https://doi.org/10.3354/
meps282237.
Huang, C.M., Liao, J.C., 1990. Response to mass selection for growth rate in Oreochromis
niloticus. Aquaculture 85, 199–205. https://doi.org/10.1016/0044-8486(90)
90019-J.
Ibáñez-Escriche, N., Blasco, A., 2011. Modifying growth curve parameters by multitrait
genomic selection. J. Anim. Sci. 89, 661–668. https://doi.org/10.2527/jas.2010-
2984.
Kamaruzzaman, N., Nguyen, N.H., Hamzah, A., Ponzoni, R.W., 2009. Growth perfor-
mance of mixed sex, hormonally sex reversed and progeny of YY male tilapia of the
GIFT strain, Oreochromis niloticus. Aquac. Res. 40, 720–728. https://doi.org/10.
1111/j.1365-2109.2008.02152.x.
Knizetova, H., Hyanek, J., Knize, B., Roubícek, J., 1991. Analysis of growth-curves of
fowl. 1. Chickens. Br. Poult. Sci. 32, 1027–1038. https://doi.org/10.1080/
00071669108417427.
Lago, A.A., Rezende, T.T., Dias, M.A.D., Freitas, R.T.F., Hilsdorf, A.W.S., 2017. The de-
velopment of genetically improved red tilapia lines through the backcross breeding of
two Oreochromis niloticus strains. Aquaculture 472, 17–22. https://doi.org/10.1016/j.
aquaculture.2016.06.042.
Lind, C.E., Safari, A., Agyakwah, S.K., Attipoe, F.Y.K., El-Naggar, G.O., Hamzah, A.,
Hulata, G., Ibrahim, N.A., Khaw, H.L., Nguyen, N.H., Maluwa, A.O., Zaid, M., Zak, T.,
Ponzoni, R.W., 2015. Differences in sexual size dimorphism among farmed tilapia
species and strains undergoing genetic improvement for body weight. Aquacult. Rep.
1, 20–27. https://doi.org/10.1016/j.aqrep.2015.03.003.
Loaiza-Echeverri, A.M., Bergmann, J.A.G., Toral, F.L.B., Osorio, J.P., Carmo, A.S.,
Mendonça, L.F., Moustacas, V.S., Henry, M., 2013. Use of nonlinear models for de-
scribing scrotal circumference growth in Guzerat bulls raised under grazing condi-
tions. Theriogenology 79, 751–759. https://doi.org/10.1016/j.theriogenology.2012.
11.031.
Mazzini, A.R.A., Muniz, J.A., Aquino, L.H., SILVA, F.F., 2003. Análise da curva de cres-
cimento de machos Hereford. Ciênc. Agrotec. 27, 1105–1112. https://doi.org/10.
1590/S1413-70542003000500019.
Mello, F., Oliveira, C.A.L., Ribeiro, R.P., Resende, Emiko K., Povh, J.A., Fornari, D.C.,
Aquaculture 511 (2019) 734243
Barreto, R.V., Mcmanus, C., Streit Jr., D., 2015. Growth curve by Gompertz nonlinear
regression model in female and males in tambaqui (Colossoma macropomum). An.
Acad. Bras. Ciênc. 87, 2309–2315. https://doi.org/10.1590/0001-
3765201520140315.
Oliveira, A.M.S., Oliveira, C.A.L., Matsubara, B.J.A., Oliveira, N.O., Kunita, N.M.,
Yoshida, G.M., Ribeiro, R.P., 2013. Padrões de crescimento de machos e fêmeas de
tilápias do Nilo (Oreochromis niloticus) da variedade GIFT. Semina: Ciênc. Agrár. 34,
1891–1900. https://doi.org/10.5433/1679-0359.2013v34n4p1891.
Oliveira, N.O., Oliveira, C.A.L., Filho, L.A., Resende, E.K., Barrero, N.M.L., Kunita, N.M.,
Santander, V.F.A., Ribeiro, R.P., 2014. Genetic parameters and morphometric char-
acteristics of two generations from the GIFT strain of the Nile Tilapia. Semina: Ciênc.
Agrár. 35, 3457–3468. https://doi.org/10.5433/1679-0359.2014v35n6p3457.
Oliveira, C.A.L., Ribeiro, R.P., Yoshida, G.M., Kunita, N.M., Rizzato, G.S., Oliveira, N.O.,
Santos, A.I., Nguyen, H.N., 2016. Correlated changes in body shape after five gen-
erations of selection to improve growth rate in a breeding program for Nile tilapia
Oreochromis niloticus in Brazil. J. Appl. Genet. 57, 487–493. https://doi.org/10.1007/
s13353-016-0338-5.
PeixeBR – Associação Brasileira da Piscicultura, 2018. Anuário PeixeBr da Piscicultura
2018. PeixeBR, Pinheiros.
Regazzi, A.J., Silva, C.H.O., 2004. Teste para verificar a igualdade de parâmetros e a
identidade de modelos de regressão não linear: dados no delineamento inteiramente
casualizado. Rev. Mat. Estat. 22, 33–45. http://jaguar.fcav.unesp.br/RME/
fasciculos/v22/v22_n3/A3_Adair.pdf.
Rutten, M.J.M., Komen, K., Bovenhuis, H., 2005. Longitudinal genetic analysis of Nile
tilapia (Oreochromis niloticus L.) body weight using a random regression model.
Aquaculture 246, 101–113. https://doi.org/10.1016/j.aquaculture.2004.12.020.
Santos, V.B., Freitas, R.T.F., Silva, F.F., Freato, T.A., 2007. Avaliação de curvas de cres-
cimento morfométrico de linhagens de tilápia do Nilo (Oreochromis niloticus). Ciênc.
Agrotec. 31, 1486–1492. https://doi.org/10.1590/S1413-70542007000500032.
Santos, V.B., Mareco, E.A., Silva, M.D.P., 2013. Growth curves of Nile tilapia (Oreochromis
niloticus) strains cultivated at different temperatures. Acta Sci. Anim. Sci. 35,
235–242. https://doi.org/10.4025/actascianimsci.v35i3.19443.
SAS Institute Inc, 2002. SAS Online Doc® 9. SAS Institute Inc., Cary.
Sousa Jr., J.A., Garrido, M.S., Carvalho, P.G.S., Rocha, L.G., Campeche, D.F.B., 2014.
Mathematical modeling applied to the growth of tilapia in net cages in the Sub
middle of the São Francisco River. Eng. Agríc. 34, 1001–1011. https://doi.org/10.
1590/S0100-69162014000500019.
Sparre, P., Venema, S.C., 1998. Introduction to Tropical Fish Stock Assessment: Part
I–Manual. FAO Fisheries Technical Paper, n. 306.1, Rev. 2. Food and Agriculture
Organization of the United Nations, Rome.
Vidal, L.V.O., Albinati, R.C.B., Albinati, A.C.L., Lira, A.D., Almeida, T.R., Santos, G.B.,
2008. Eugenol como anestésico para tilápia-do-nilo. Pesq. Agropec. Bras. 43,
1069–1074. https://doi.org/10.1590/S0100-204X2008000800017.