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Variation of age and total length in Sotalia guianensis (Van Beneden, 1864) (Cetacea, Delphinidae), on the coast of Espirito Santo state, Brazil/ Variacao etaria e de comprimento total de Sotalia guianensis (Van Beneden, 1864) (Cetacea, Delphinidae), no Litoral do Espirito Santo, Brasil.

1. Introduction

The Guiana dolphin (Sotalia guianensis, Van Beneden, 1864) is found along the tropical and subtropical Atlantic coast of the South and Central Americas, from Honduras (Edwards and Schnell, 2001) to the state of Santa Catarina, Brazil (Simoes-Lopes, 1988). Although it is one of the species that have been most studied in these regions, it is still considered insufficiently known by the International Union for Conservation of Nature (IUCN, 2003) and by the Brazilian environmental authorities (IBAMA, 2001 ).

Variations in growth pattern may be associated with seasonal changes, environmental factors, competition strategies, and patterns of reproduction investment (Amano and Miyazaki, 1992). Intraspecific morphological changes represent an important source of information in the identification of the variability of geographical and non-geographical elements. Currently, several types of data are used to identify populations. Studies about phenotypical characters (osteology, morphology, and pigmentation patterns) based on multivariate techniques have been consistently carried out to identify populations in several taxonomic groups (Wang et al., 1999).

Age estimates of cetaceans stand is a good tool to characterize populations and to understand the biology of individuals (Pinedo and Hohn, 2000; Butti et al., 2007; Azevedo et al., 2015; Carvalho et al., 2015). In this sense, the ability to estimate the age of small cetaceans is extremely important in natural history studies (Hohn et al., 1989).

The present study determined age and morphology variations in the Guiana dolphin in the state of Espirito Santo, Brazil.

2. Material and Methods

In total, 44 specimens of S. guianensis accidentally captured in fisheries or stranded in the state of Espirito Santo, Brazil, were used. Detailed information on specimens recovered and used in this study are provided in Table 1. Individuals were found between Conceiqao da Barra (18[degrees]30'S), and Presidente Kennedy (21[degrees]05'S), farther south. Initially, total length (TL) and sex of animals were established. Next, teeth were extracted to estimate age. The teeth whose roots were straight and that exhibited the lowest degree of wear of crown were chosen, independently of their position in the mandibles. The method described by Hohn et al. (1989) was adopted. At first, teeth were cut to 3-mm to 5-mm-thick sections parallel to the longest bucco-lingual axis using a low-speed metal saw equipped with diamond blades. Sides of sections were also removed to improve the action of the decalcification agent and facilitate the subsequent sectioning of tooth specimens using a microtome-cryostat. Tooth sections were soaked in a quick-action commercial decalcification agent containing HCl (RDO[TM]) for periods between 3 h and 24 h, depending on the size of sections and on the degree pulpar cavities were filled. The ideal degree of decalcification was established when sections were completely flexible. Decalcified specimens were sectioned again parallel to the longest axis in a microtome-cryostat. Central sections were chosen so as to afford more accurate age readings. Sections were stained using Mayer's hematoxylin to reveal growth layers groups (GLGs). Readings were made in an optical microscope under 40x magnification.

Descriptive statistics was used for mean, maximum, minimum, and standard deviation of total length values. Animals were sorted by dental age as immature ([less than or equal to] 6 years) and mature ([greater than or equal to] 7 years), and by sex. Inferential statistics included the calculation of growth parameters for TL and predicting the asymptote based on the Gompertz non-linear model, Y = ae[-e (b-cx)], where Y is the measured variable, a is the asymptote, b is the correction factor, c is the growth rate constant, and x is the age (Zullinger et al., 1984). The model was adjusted using the Curve Expert 1.4 software for Windows.

3. Results

The age of 44 S. guianensis specimens was estimated (see Figure 1). Values were between 0.5 year and 33 years (mean = 8.34, SD = 7.06). Most specimens (47%) were between zero and 6 years.

Age of immature males ranged from 1 year to 6 years (mean = 3.08, SD = 1.97), while mature males were between 8 and 23 years old (mean = 12.45, SD = 4.92). Immature females varied between 0.5 year and 4 years of age (mean = 2.5, SD = 1.32), and age of mature females ranged from 7 to 33 years (mean = 15.75, SD = 8.20) (as shown in Table 2).

The age-based TL growth curve constructed using the Gompertz model indicated that asymptotic lengths was reached at 182 cm, roughly in the 5-6 years age range (correction factor = -0.54, growth rate = 0.79, coefficient of determination, [R.sup.2] = 0.82) (see Figure 2).

The growth curve for TL (cm) and age (years) adjusted with the Gompertz model for male S. guianensis specimens indicated that asymptotic length was reached at approximately 176 cm (correction factor = 1.28, growth rate = 2.68, coefficient of determination, [R.sup.2] = 0.71) (see Figure 3). For S. guianensis females, asymptotic length was reached at 191 cm (correction factor = -0.44, growth rate = -0.54, coefficient of determination, [R.sup.2] = 0.96) (Figure 4).

Mean TL for immature males ([less than or equal to] 6 years) was 166.11 cm (SD = 20.34). For mature males ([greater than or equal to] 7 years), mean TL was 190.18 cm (SD = 158.75). For immature and mature females mean TL was 158.75 cm (SD = 28.19) and 191.0 cm (SD = 7.12) (as shown in Table 3).

4. Discussion

Previous studies reported lower age variation ranges for S. guianensis in Espirito Santo, Brazil, compared with the values obtained in the present research(mean age = 8.34 years, SD = 7.06, minimum = 0.5 year, maximum = 33 years). Ramos et al. (2000) analysed S. guianensis found in the north of the state of Rio de Janeiro, Brazil, and suggested that adults may reach the age of 30 years. For Rosas et al. (2003) S. guianensis may live for up to 35 years, though the oldest male observed in their study on the coast of the state of Parana, Brazil, was 29 years old.

In the present study, age of males varied between 1 and 23 years, while for females the age range was 0.5 year (newly born) to 33 years. Di Beneditto and Ramos (2004) observed that age range was zero--21 years for males and 0.5-33 years for females in northern Rio de Janeiro state, Brazil. Lailson-Brito et al. (2010) reported that maximum age for S. guianensis was 14 years for one male in Guanabara Bay, 13 years for one male in Sepetiba Bay, and 20 years for one female in Paranagua Bay, all of which are in Brazil. These values are similar, and suggest higher life expectancy for females of the species.

Rosas et al. (2003) believe that young S. guianensis individuals as well as those in the process of reaching sexual maturity (between 4 and 6 years of age) are more susceptible to be captured. Similarly, Di Beneditto and Ramos (2004) reported that males of up to 6 years of age account for 80% of S. guianensis captured, and suggest that individuals at the beginning of the sexual maturation stage are more vulnerable. For the authors, such vulnerability may be associated with behaviour pattern and composition of populations. In the present study, the age group to which the highest number of animals (47%) belonged was zero--6 years, which confirms that younger animals at the sexual development stage are more vulnerable to being accidentally captured by fish nets. Significant social organization issues may lead to differential vulnerability based on age groups and sex (IWC, 1994). The excessive decline in populations could indicate a change in the ecosystem (Taylor, 1997). The fact that most animals accidentally captured were at reproductive stage may play a role in population decline, though no in-depth study has evaluated the risks S. guianensis is exposed to. Due to the threats faced by the specimens, it has been has suggested that the species should be considered vulnerable, in light of the threats it has had to face (Rosas, 2006).

Using the Von Bertalanfy method, Schmiegelow (1990) estimated that TL asymptote of S. guianensis was 182.6 cm in the Brazilian states of Sao Paulo and Parana. Santos et al. (2003) used the same method to analyse S. guianensis specimens from the same states and reported maximum TL of 186.4 cm. Rosas et al. (2003) analysed S. guianensis from the state of Parana using the Von Bertalanfy method and observed that males and females reached 186.4 cm and 177.3 cm in TL, respectively. However, the authors noticed that growth of males may be discontinuous at the age of 5 years, with a secondary growth process at puberty, which required that separate growth curves for sexes. The Gompertz model is often employed in small cetacean morphology studies (Fernandez and Hohn, 1998; Ramos et al., 2000, 2010; Di Beneditto and Ramos, 2004). Di Beneditto and Ramos (2004) used the Gompertz model to conclude that maximum TL was 191 cm for S. guianensis in northern Rio de Janeiro, a value that is higher than that observed in the other study sites mentioned. Such difference in asymptotic TL may be the result of regional variation between populations. However, in the present study the asymptotic TL value was near the mean value, when compared with the other regions surveyed. TL of 44 S. guianensis individuals varied between 119 cm ad 200 cm, with mean of 174.10 cm and SD of 20.51 cm.

Ramos et al. (2010) reported that TL of S. guianensis from the state of Espirito Santo varied between 175.0 and 222.0 cm for males and 166.0 and 184.5 cm for females. For mature individuals TL varied between 167.0 and 222.0 cm, similarly to the values observed in the present study. In the north of the state of Rio de Janeiro, TL of males varied between 86.0 and 200.0 cm, while TL of females ranged from 117.5 and 198.0 cm. TL of mature individuals varied between 161.0 and 200 cm. The specimens evaluated in the state of Sao Paulo presented mean TL values that were shorter than those of S. guianensis from Rio de Janeiro and Espirito Santo (Ramos et al., 2010). As observed by Ramos et al. (2010), length obeys a clinal gradient that increases with latitude and, under specific conditions, factors other than heat conservation may affect geographic variation, such as nutrition requirements.

Variations in TL of S. guianensis were observed across its distribution range. The largest individual observed was a female found stranded on the coast of Espirito Santo measuring 206.0 cm (Barros, 1991). Di Beneditto and Ramos (2004) recorded maximum TL of 200 cm for a male and 198 cm for a female in the north of Rio de Janeiro state. Lailson-Brito et al. (2010) observed that maximum TL of S. guianensis in Guanabara Bay was 191 cm, while TL of animals from the Sepetiba and Paranagua bays were 195 cm and 198 cm, respectively. However, Barbosa and Barros (2006) estimated TL values and declared that maximum TL for the species would be 222 cm. For the state of Espirito Santo, maximum TL was observed in the present study were 200 cm for females and 198 cm for males, though age of individuals was not assessed. TL data obtained here were similar to those cited above.

The S. guianensis individuals found on the coast of the state of Espnito Santo, Brazil had higher mean TL than animals surveyed in other locations. Variation in TL between animals of different regions was discussed by Cunha et al. (2010), who described changes in the parameter across animals of various geographic regions using DNA analysis that indicated distinct S. guianensis populations in the states of Para, Ceara, Rio Grande do Norte, Bahia, Espirito Santo, and in the southeast and south states (Rio de Janeiro, Sao Paulo, Parana e Santa Catarina). Similarly, Caballero et al. (2006) pointed to the differences between Caribbean and South and Central American specimens. However, the same authors observed small genetic differences between populations living on the Brazilian coast (Caballero et al., 2010).

Most morphometric studies with cetaceans used cranium and skeleton parameters (Perrin et al., 2003). Little research has used external morphological parameters, possibly due to the difficulty to obtain samples. Also, some characters are affected by changes occurred after the animal died, especially due to decomposition (Wang et al., 2000).

Age estimates based on GLGs are a useful tool in the determination of sexual maturity and development stage of individual. In like manner, studies about the degree of morphological, genetic, or behavioral changes in cetaceans afford to better understand the evolutive processes underwent by one species, and are useful in the management of populations (Wiig, 1992). Younger animals are more susceptible to being captured accidentally, especially males, which highlights the importance of studies and of monitoring programs in conservation efforts for this species.

http://dx.doi.org/10.1590/1519-6984.13215

Acknowledgements

The authors are grateful to Coordenafao de Aperfeifoamento de Pessoal de Nivel Superior (CAPES) and ORCA institute for allowing using the samples that enabled the conduction of this study.

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J.Y. Lima (a), *, A.P.M. Carvalho (a), C.T. Azevedo (a), L.A. Barbosa (b), L.S. Silveira (a)

(a) Laboratorio de Morfologia e Patologia Animal, Universidade Estadual do Norte Fluminense Darcy Ribeiro--UENF, Av. Alberto Lamego, 2000, Parque California, CEP 28016-000, Campos dos Goytacazes, RJ, Brazil

(b) Instituto ORCA, Rua Sao Paulo, 23, Praia da Costa, CEP 29101-315, Vila Velha, ES, Brazil

* e-mail: ju.ywasaki@gmail.com

Received: August 24, 2015--Accepted: March 28, 2016--Distributed: August 31, 2017 (With 4 figures)

Caption: Figure 1. Age (years) frequency of Sotalia guianensis in the state of Espirito Santo, Brazil.

Caption: Figure 2. Growth curve adjusted with the Gompertz model for total length (cm) and age (years) for Sotalia guianensis specimens in the state of Espirito Santo, Brazil.

Caption: Figure 3. Growth curve adjusted with the Gompertz model for total length (cm) and age (years) for male Sotalia guianensis specimens in the state of Espirito Santo, Brazil.

Caption: Figure 4. Growth curve adjusted with the Gompertz model for total length (cm) and age (years) for female Sotalia guianensis specimens in the state of Espirito Santo, Brazil.
Table 1. Sotalia guianensis data used in this study. Information
includes specimen identification, collection date, sex (male: M,
female: F, UN: unknown sex), total length (cm), locality, city,
tissues samples stored and responsible staff. All tissues samples
were stored at the ORCA institute's head office.

Specimen   Collection   Sex   Total    Locality         City
           date               length

SOT.05     18/03/1996   F     189      Itaparica        Vila Velha
SOT. 19    09/03/2003   M     189      Jacaraipe        Serra
SOT.23     06/10/2003   M     172      Santa Cruz       Aracruz
SOT.30     04/04/2004   M     196      Siribeira        Guarapari
SOT. 31    04/05/2004   UN    183      Meaipe           Guarapari
SOT.37     12/09/2004   UN    189      Formosa          Aracruz
SOT.42     01/09/2004   F     200      Ponta da Fruta   Vila Velha
SOT.44     19/11/2004   UN    187      Santa Cruz       Aracruz
SOT.45     06/04/2005   M     166      Regencia         Linhares

SOT.46     06/04/2005   M     173      Regencia         Linhares
SOT.48     27/06/2005   F     162      Ilha do Boi      Vitoria
SOT. 52    10/01/2006   M     169      Regencia         Linhares
SOT. 53    16/01/2006   M     169      Regencia         Linhares
SOT.56     01/03/2006   M     158      Regencia         Linhares
SOT.57     14/03/2006   F     196      Setiba           Guarapari
SOT. 58    17/03/2006   M     190      Ilha do Frade    Vitoria
SOT.62     02/01/2007   F     195      Costa            Vila Velha

SOT.64     17/01/2007   M     198      Mae-Ba           Anchieta

SOT.66     22/01/2007   M     185      Barrinha         Vila Velha

SOT.70     15/03/2007   F     185.5    Costa            Vila Velha

SOT.72     06/04/2007   M     190      Morada do Sol    Vila Velha

SOT.73     09/04/2007   M     167      Regencia         Linhares

SOT.79     11/06/2007   UN    189      Guriri           Sao Mateus
SOT.83     12/01/2007   F     183      Regencia         Linhares

SOT. 84    12/10/2007   M     144.5    Regencia         Linhares

SOT.85     18/10/2007   M     151.5    Itapua           Vila Velha

SOT. 86    27/11/2007   F     192.5    Santa Cruz       Aracruz

SOT.88     20/01/2008   F     151.5    Centro           Conceijao
                                                        da Barra

SOT. 92    08/03/2008   F     185      Manguinhos       Serra

SOT.93     10/03/2008   F     183      Jacaraipe        Serra
SOT.94     28/03/2008   F     169      Regencia         Linhares

SOT.96     28/04/2008   M     190      Peracanga        Guarapari

SOT.99     21/08/2008   F     119      Regencia         Linhares

SOT 103    08/12/2008   M     187      Solemar          Serra
SOT 110    20/03/2009   UN    149      Setiba           Guarapari

SOT 113    29/03/2009   M     165      Regencia         Linhares

SOT 115    03/05/2009   M     164      Areia Preta      Guarapari

SOT 118    27/07/2009   M     165      Guaibura         Guarapari

SOT 119    06/08/2009   M     180      Castelhanos      Anchieta

SOT. 120   15/08/2009   M     129      Siribeira        Guarapari

SOT 123    06/12/2009   M     140      Castelhanos      Anchieta

SOT. 125   21/12/2009   M     161.3    Regencia         Linhares

SOT 131    17/04/2010   M     122      Mae-Ba           Anchieta

SOT 133    07/06/2010   M     174      Itaipava         Itapemirim

Specimen   Tissues samples stored                        Responsible
                                                         staff

SOT.05     Skeleton, teeth                               L. Barbosa
SOT. 19    Skeleton, teeth                               L. Barbosa
SOT.23     Skeleton, teeth                               L. Barbosa
SOT.30     Skeleton, teeth                               L. Barbosa
SOT. 31    Skeleton, teeth                               L. Barbosa
SOT.37     Skeleton, teeth                               L. Barbosa
SOT.42     Skeleton, teeth                               L. Barbosa
SOT.44     Skeleton, teeth                               L. Barbosa
SOT.45     Skeleton, teeth, lung, bone marrow, muscle,   L. Barbosa
           liver, brain
SOT.46     Skeleton, teeth, liver, lung, muscle          L. Barbosa
SOT.48     Skeleton, teeth, liver, bone marrow, lung     L. Barbosa
SOT. 52    Skeleton, teeth, bone marrow, muscle          L. Barbosa
SOT. 53    Skeleton, teeth, muscle, liver, bone marrow   L. Barbosa
SOT.56     Skeleton, teeth, muscle, liver, bone marrow   L. Barbosa
SOT.57     Skeleton, teeth, muscle                       L. Barbosa
SOT. 58    Skeleton, teeth, muscle, liver                L. Barbosa
SOT.62     Skeleton, teeth, muscle, lung, intestine      L. Barbosa
           proximal, distal bowel
SOT.64     Skeleton, teeth, lung, intestine proximal,    L. Barbosa
           distal bowel
SOT.66     Skeleton, teeth, muscle, lung, liver,         L. Barbosa
           intestine proximal
SOT.70     Skeleton, teeth, lung, kidney, muscle,        M. Araujo
           liver, intestine proximal, distal bowel
SOT.72     Skeleton, teeth, brain, bone marrow, lung,    L. Serafim
           muscle, intestine proximal, distal bowel
SOT.73     Skeleton, teeth, lung, brain, kidney,         M. Araujo
           liver, muscle, intestine proximal, distal
           bowel
SOT.79     Skeleton, teeth                               I. Bianchi
SOT.83     Skeleton, teeth, muscle, kidney, liver,       I. Bianchi
           adipose, intestine proximal, distal bowel
SOT. 84    Skeleton, teeth, liver, lung, adipose,        I. Bianchi
           kidney, intestine proximal, distal bowel
SOT.85     Skeleton, teeth, lung, kidney, adipose,       M. Araujo
           liver, intestine proximal, distal bowel
SOT. 86    Skeleton, teeth, lung, kidney, liver,         I. Bianchi
           muscle, adipose, intestine proximal, distal
           bowel
SOT.88     Skeleton, teeth, lung, kidney, muscle,        I. Bianchi
           liver, adipose, intestine proximal,
           distal bowel
SOT. 92    Skeleton, teeth, kidney, muscle, lung,        L. Serafim
           liver, adipose, intestine proximal, distal
           bowel
SOT.93     Skeleton, teeth                               L. Serafim
SOT.94     Skeleton, teeth, liver, lung, kidney,         I. Bianchi
           muscle, adipose, intestine proximal, distal
           bowel
SOT.96     Skeleton, teeth, lung, bone marrow, liver,    I. Bianchi
           muscle
SOT.99     Skeleton, teeth, muscle, kidney, adipose,     L. Barbosa
           liver, intestine proximal, distal bowel
SOT 103    Skeleton, teeth                               L. Serafim
SOT 110    Skeleton, teeth, adipose, liver, lung,        L. Serafim
           muscle
SOT 113    Skeleton, teeth, muscle, lung, kidney,        I. Bianchi
           liver, adipose, intestine proximal, distal
           bowel
SOT 115    Skeleton, teeth, muscle, liver, intestine     L. Serafim
           proximal, distal bowel
SOT 118    Skeleton, teeth, liver, adipose, muscle,      L. Serafim
           kidney, intestine proximal, distal bowel
SOT 119    Skeleton, teeth, muscle, lung, kidney,        L. Serafim
           liver, testicle, intestine proximal, distal
           bowel
SOT. 120   Skeleton, teeth, muscle, liver, adipose,      I. Bianchi
           lung, kidney, intestine proximal, distal
           bowel
SOT 123    Skeleton, teeth, muscle, kidney, lung,        L. Barbosa
           adipose, intestine proximal, distal bowel
SOT. 125   Skeleton, teeth, muscle, kidney, lung,        L. Serafim
           adipose, intestine proximal, distal bowel
SOT 131    Skeleton, teeth, liver, kidney, adipose,      L. Serafim
           muscle, lung, intestine proximal, distal
           bowel
SOT 133    Skeleton, teeth                               L. Serafim

Table 2. Maximum, minimum, mean, and standard deviation of age (years)
of mature and immature male and female Sotalia guianensis specimens in
the state of Espirito Santo, Brazil.

                     Males               Female
                     Immature   Mature   Immature   Mature

Minimum              1          8        0.5        7
Mean                 3.08       12.45    2.5        15.75
Maximum              6          23       4          33
Standard deviation   1.97       4.92     1.32       8.20

Table 3. Maximum, minimum, mean, and standard deviation of total
length (cm) of mature and immature male and female Sotalia guianensis
specimens in the state of Espirito Santo, Brazil.

                     Males               Females
                     Immature   Mature   Immature   Mature

Minimum              129        158      119        183
Mean                 166.11     180.18   158.75     191
Maximum              190        198      185        200
Standard deviation   20.34      13.68    28.19      7.12
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Title Annotation:Original Article
Author:Lima, J.Y.; Carvalho, A.P.M.; Azevedo, C.T.; Barbosa, L.A.; Silveira, L.S.
Publication:Brazilian Journal of Biology
Date:Jul 1, 2017
Words:4869
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