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.
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.
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).
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.
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: firstname.lastname@example.org
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|
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