Sexual Dimorphism in the Turtle Kinosternon Scorpioides (Testudines: Kinosternidae) from Marajó Island, Brazilian Amazon
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Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(2): 601-614, April-June 2021 (Published May 14, 2021) 601 Silva da Silva, J., dos Santos Braga, B.S., da Silva Costa, J., Schlemmer Brasil, L., Lobato de Oliveira-Bahia, V.R., Pimentel Leal, R., Felipe Marques, J.R., & de Araújo Guimarães, D.A. (2021). Sexual dimorphism in the turtle Kinosternon scorpioides (Testudines: Kinosternidae) from Marajó Island, Brazilian Amazon. Revista de Biología Tropical, 69(2), 601-614. https://doi.org/10.15517/rbt. v69i2.42834 https://doi.org/10.15517/rbt.v69i2.42834 Sexual dimorphism in the turtle Kinosternon scorpioides (Testudines: Kinosternidae) from Marajó Island, Brazilian Amazon Joilson Silva da Silva1 Brenda Stefany dos Santos Braga1 Juliane da Silva Costa1* Leandro Schlemmer Brasil1 Verônica Regina Lobato de Oliveira-Bahia1 Relionan Pimentel Leal2 José Ribamar Felipe Marques2 Diva Anélie de Araújo Guimarães1 1. Institute of Biological Sciences, Universidade Federal do Pará, Belém, Pará, Brazil; [email protected], [email protected], [email protected] (*Correspondence), [email protected], [email protected], [email protected] 2. Empresa Brasileira de Pesquisa Agropecuária, Embrapa Amazônia Oriental, Belém, Pará, Brazil; [email protected], [email protected] Received 08-VII-2020. Corrected 06-II-2021. Accepted 22-IV-2021. ABSTRACT Introduction: Morphometrics analysis is an efficient and low-cost technique used in studies of sexual dimor- phism in turtles. Kinosternon scorpioides scorpioides, scorpion mud turtle, has a wide phenotypic variation, depending on the area of its occurrence. Objective: The objective of this work was to identify the anatomical sexual difference of K. s. scorpioides, adults and hatchlings, through morphometric analysis; and relate the weights of adult animals to environmental factors (temperature and rainfall) in Marajó Island, Brazil. Methods: The sample collection was carried out from March to September 2018, covering both the rainy season (January to July) and the dry season (August to December). For the biometric analysis, 95 adults and 21 hatchlings were used, in which the length and width of the carapace and plastron, height of the shell, and weight were measured (adults only). For the geometric morphometry analysis, 21 adults and 13 hatchlings were used, in which 27 coor- dinates of anatomical landmarks were inserted in each image of the carapace and 11 in the plastron. Hatchlings were sexed by histology which was enabled by the identification of the ovaries and testicles. Results: The results showed the existence of dimorphism in adults. The plastron and height were higher in females, which had a more rounded carapace than males. This characteristic may be related to the species’ sexual strategy, where males impose copulation. Histologically, it was possible to identify the ovaries and testicles in the hatchlings, but there was no anatomical sexual difference, despite the tendency to differentiate in the analysis of carapace PCA. Conclusions: Sexual dimorphism in K. s. scorpioides may play an important role on its reproductive behavior, which is synchronized with environmental events. This fact suggests that the reproductive strategies of this spe- cies would be severely affected by changes in the ecosystem. Key words: biometrics; geometry morphometrics; scorpion mud turtle; sexual difference; turtles. 602 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(2): 601-614, April-June 2021 (Published May 14, 2021) The turtles or Testudines are represented & Iverson, 2011). This species is one of the by 356 species, and considering the subspecies, smallest turtles of the Amazon forest, measur- they total 478 modern taxa, divided into 13 ing from 18 to 27 cm in length (Vogt, 2008). families (Rhodin et al., 2017). Of this total, 20 Its conservation status in the Brazilian terri- % are found in South America (Souza, 2004; tory is categorized as least concern (Vogt et Ferreira-Júnior, 2009). Thirty-six species are al., 2015), despite it being the only species of known in Brazil (Costa & Bérnils, 2018), out the Kinosternidae family occurring in Brazil of which 17 terrestrial species have been iden- (Viana, Santos, & Antunes, 2015). It is severely tified in the Brazilian Amazon, 15 aquatic and exploited by illegal consumption and trade in two terrestrial species. many places (Ferrara et al., 2016), especially Studies on the biological processes related in Marajó island, State of Pará, Brazil (Cristo, to the growth, change in the size, shape and Baía-Júnior, Silva, Marques, & Guimarães, body pattern of turtles, can be carried out 2017). In addition, there are few conservation through morphometric analysis of the carapace and management programs for this species. and plastron. This technique has been applied This animal is well adapted to captive condi- to distinguish morphological variations by ana- tions; however, it is necessary to expand the tomical landmarks (Monteiro & Reis, 1999), knowledge about its nutritional requirements proving to be accurate for phylogenetic stud- and management (Costa et al., 2017). In this ies and sexual differentiation of these animals instance, there is little information of the (Valenzuela, Adams, Bowden, & Gauger, 2004; aspects regarding the reproductive biology Depecker, Berge, Penin, & Renous, 2006; of the free-living species. Nevertheless, it is Ferreira-Júnior, Treichel, Scaramussa, & Scal- known that they copulate on land and in shal- foni, 2011; Sönmez, Bağda, Candan, & Yilmaz, low waters. Their nests are found at the base 2019). Morphological analyses allow research- of the roots of shrubs, away from water bodies ers to precisely identify the shape and size of (Ferrara et al., 2016). Sex is determined by the biological organisms, allowing the observa- temperature of incubation during embryonic tion of their morphological changes (Van Der development (Ewert & Nelson, 1991; Rueda- Molen, Martínez-Abadía, & González, 2007). Almonacid et al., 2007), and sexual maturity is It has as an advantage of increasing the feasi- attained when the animal reaches 2.8 to 5 years bility of collecting samples, as only an analysis old (Vogt, 2008). of the photograph of the animal is necessary The phenotypic difference between adult (Lyra, Hatadani, Azeredo-Espin, & Klaczko, males and females, raised in captivity, is related 2010). It is important to understand that most to body size, plastron shape, weight, tail size of the techniques used in sexing chelonian and pigmentation in the male’s head (Castro, hatchlings are largely impractical and invasive, 2006). The adult female measures an aver- even requiring to slaughter the animal (Valen- age of 15.26 cm in length and 430.08 g in zuela et al., 2004). Therefore, it is necessary to weight, and the male 14.79 cm and 314.05 apply non-invasive techniques, to differentiate g, respectively (Castro, 2006). Generally, the the sex of the hatchlings. Sexing is a useful tool first nesting occurs, when the female reaches in management practices in the wild or captiv- 10 cm in carapace length (Barreto, Lima, & ity, enabling the correct intervention for the Barbosa, 2009). In males, sexual maturity is reintroduction and release of animals, or in the reached at 10 cm (Barreto et al., 2009) to 13.2 formation of groups. cm in carapace length (Vogt, 2008). However, The scorpion mud turtle (Kinosternon a variation in the body size has been found in scorpioides scorpioides) is geographically dis- the wild, where males may be larger or smaller tributed from Panama to Argentina and inhab- in relation to females (Berry & Iverson, 2011). its permanent, semi-permanent and temporary Hatchling turtles in captivity are on average 2.6 aquatic environments (Iverson, 2010; Berry cm long and weigh 2.8 g (Costa et al., 2017). Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(2): 601-614, April-June 2021 (Published May 14, 2021) 603 They do not show any apparent sexual dimor- collected from the scientific research breed- phism until they reach 20 months of age (9.4 ing facility of Empresa Brasileira de Pesquisa cm in length), when there is an increase in the Agropecuária - Embrapa Amazônia Oriental tail and the presence of pigmentation on the (License number 7310/2014-SEMAS-PA), head of the males (Castro, 2006). located in Salvaterra, Marajó island, Pará, Bra- Thus, the main objective of this research zil, (0°42’26.90” S & 48°33’34.70” W) (Fig. was to identify the sexual morphological differ- 1). In addition to the 13 samples, more eight ence of K. s. scorpioides through the morpho- hatchlings were also obtained for biometry, a metric analysis of adult animals and hatchlings total of 21 animals. Hatchlings were sexed by turtles, in addition to relating the weight mea- histological analysis of the gonads. The testi- surements of adult animals to environmental cles and ovaries were fixed in Bouin’s solution factors (temperature and rainfall) in Marajó and preserved in 70 % alcohol. The samples island, Pará, Brazil. were dehydrated in an increasing ethanolic solution (70, 80, 90 and 100 %), diaphanized in MATERIALS AND METHODS xylol and included in paraffin. Posteriorly, his- tology sections 5 µm were stained with Hema- Data collection: Samples from 95 wild toxylin and Eosin, and the slides were analyzed adults K. s. scorpioides, for traditional mor- with optical microscopy. phometrics (biometrics) and weight analy- The research performed were approved sis, were collected in Cachoeira do Arari, by the Chico Mendes Institute for Biodiver- Mesoregion of Marajó island, Pará, Brazil, sity Conservation (ICMBio-SISBIO 59314-1), specifically in Guajarás farm (0°37’7.50” S & the Ethics Committee for Animals Research 48°58’59.68” W) (Fig. 1). The animals were - Universidade Federal do Pará (Authorization captured manually in the wild, followed by number CEUA 7749240817), and the Ethics release. No anesthetic was used, with a short Committee for Use of Animals - Embrapa physical containment time. In addition, photo- (Authorization number 001-2016). identification technique of the animal’s head was used for records, as it has different marks, Morphometrics: Ninety-five adults scor- avoiding recapture.