Biometric and Sexual Dimorphism Variation of Hydromedusa Tectifera in Brazil
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Basic and Applied Herpetology 34 (2020) 47-57 Biometric and sexual dimorphism variation of Hydromedusa tectifera in Brazil Priscila da Silva Lucas1,4, Júlio César dos Santos Lima2,*, Aline Saturnino Costa1, Melise Lucas Silveira3, Alex Bager1 1 Brazilian Center for Studies in Road Ecology (CBEE), Ecology Sector, Department of Biology, Federal University of Lavras, University Campus, Mailbox 3037, Lavras, MG CEP 37200-000, Brazil. 2 Postgraduate Program in Environmental Engineering Sciences, Center for Water Resources and Environ- mental Studies (CRHEA) - São Carlos School of Engineering - University of São Paulo, Rodovia Domin- gos Inocentini, Km 13,5, Itirapina, SP CEP 13530-000, Brazil. 3 Vertebrate Laboratory, Institute of Biological Sciences, Federal University of Rio Grande, Rio Grande, RS CEP 96203-900, Brazil. 4 Present Address: Laboratório de Ciências Ambientais, Universidade Estadual Norte Fluminense Darcy Ribeiro, CEP 28035-200, Campos dos Goytacazes, Rio de Janeiro, Brazil. *Correspondence: E-mail: [email protected] Received: 30 March 2020; returned for review: 11 May 2020; accepted 22 June 2020. Body size has a strong influence on the ecology and evolution of organisms’ life history. Turtle species can exhibit variation in body size and shape between populations of conspecifics through usually broad geographical scales. This prediction is timely to be tested in this study with the spe- cies Hydromedusa tectifera. We aimed to evaluate the variation in body size between and sexual dimorphism within populations of H. tectifera in two areas in Brazil. Sampling occurred in Minas Gerais and Rio Grande do Sul states in order to obtain morphometric measures of carapace and plastron of the individuals. We observed sexual dimorphism within populations. In Rio Grande do Sul state, females were larger than males in most of the carapace and plastron measures. In Minas Gerais state, males were larger than females regarding maximum carapace width. Overall, individ- uals from Rio Grande do Sul state were larger than those from Minas Gerais state. We discuss pos- sible factors that might cause variation in morphology within and between populations of conspe- cifics. Research on morphology is encouraged to facilitate comparisons among populations in geo- graphically broad areas. Key words: Body size; geographic variation; South America; turtle. Body size and related measures influ- evolutionary units in nature (Dos-Reis et ence many aspects of life history and evo- al., 2002). The knowledge of this variation lution of animals (LaBarbera, 1989; Meiri, plays an important role in the implementa- 2008). Morphological studies not only ana- tion of taxonomic studies (Rohlf Mar- lyze shape variations but also try to clarify cus, 1993), with the investigation of the their causes and effects (Bookstein, 1991). possible occurrence of new characters or Whether among or within species’ popula- the change in morphology of the current tions, the description of morphological ones. variation patterns is essential to highlight In freshwater turtle species variation in DOI: http://dx.doi.org/10.11160/bah.182 DA SILVA LUCAS ET AL. body size and shape between populations SSD decreased with increasing latitude of conspecifics is widely recognized, usu- and was slightly higher inland than in ally in broad geographical scales (Ashton coastal areas, for males and females of et al., 2007; Daza Páez, 2007; Zuffi et al., Chrysemys picta, in North America. Other 2007). Many explanations have already studies have also evaluated SSD in turtles been hypothesized, and the main ones in terms of geographic variation, such as comprise differences in resource availabil- Lovich et al. (1998; 2010), for Clemmys ity and quality, population density, envi- muhlenbergii and Mauremys leprosa, Zuffi et ronmental conditions (such as temperature al. (2006) for Emys orbicularis and Emys tri- and seasonality), and hunting intensity nacris in Italy. For the species Clemmys (Rowe, 1994; Ashton et al., 2007; Daza guttata, Rowe et al. (2012) studied sexual Páez, 2007). In this group, there is a trend dimorphism in relation to the size and for larger body size in higher latitude (i.e. shape of the carapace and dichromatism in decreased environmental temperature) southwest Michigan (USA). Basic (Ashton Feldman, 2003) known as the knowledge of life history traits are essen- traditional ecogeographic Bergmann’s rule tial and represent the first, necessary, steps (Mayr, 1956). The Bergmann’s rule as- for a deeper understanding in order to sumes that larger individuals conserve apply management and conservation prac- heat better in cooler than in warmer areas tices (Daza Paéz, 2007). (Ashton et al., 2007). Most turtle families Hydromedusa tectifera Cope, 1870 is a that include terrestrial and semi-aquatic medium-sized turtle belonging to the fam- species such as the Chelydridae, Emydi- ily Chelidae with distribution in South- dae, Kinosternidae and Testudinidae fol- -Southern Brazil, Paraguay, Uruguay, Ar- low this trend (Zuffi et al., 1999, Ashton gentina and Bolivia (Fritz Havas, 2007; Feldman, 2003). This pattern is also found van Dijk et al., 2014). Knowledge of the in species of the Chelidae family such as ecology and biology of this species is Acanthochelys spixii in Brazil (Bager et al., punctual. Clutch size averaged 11.6 eggs 2016). However, for many turtle species, per year at the Taim Ecological Station, incipient knowledge about morphology, extreme south of Brazil (Fagundes population ecology and reproductive biol- Bager, 2007). Population density may ogy at local scales is still lacking. There- reach 218 individuals ha -1 and turtle peak fore, a comprehensive survey at broader of activity is in spring and summer in Ar- scales for testing this kind of ecological gentina (Lescano et al., 2008) and Brazil. hypothesis become unfeasible. Its diet is based mainly on leeches, anne- This is also true for information about lids, gastropods, arachnids, insects, and sexual size dimorphism (SSD). For in- fishes (Lescano et al., 2009 , Alcalde et al., stance, Lovich et al. (1998) found that 2010). males are larger than females in Glyptemys To our knowledge, only Clavijo- muhlenbergii regardless of the location of Baquet et al. (2010) provided evidence the populations sampled at varying lati- about morphological variation among in- tudes. Litzgus Smith (2010) found that dividuals from three different watershed 48 MORPHOLOGICAL VARIATION IN HYDROMEDUSA TECTIFERA basins across the distribution of Hydrome- pling occurred in three close locations of dusa tectifera. Adapted to a wide gradient streams and estuarine swamps. The cli- of environmental conditions, species are a mate in these locations are classified as good model for testing hypotheses about humid subtropical (hot and wet summers morphological variation on a broader scale and mild, drier winter) and the average in Brazil. Therefore, we aimed at answer- annual temperature varies between 18 to ing the following questions: 1) Can we 19°C (Matzenauer et al., 2011). observe sexual size dimorphism between Data collection males and females within populations of H. tectifera? We expected males to be larger Turtles were captured in four locations than females in accordance with the gen- (three in Rio Grande do Sul and one in eral pattern of sexual size dimorphism for Minas Gerais state) (Table 1). Each indi- family Chelidae, mainly in the measure- vidual was measured for six linear mor- ments related to plastron size that are fa- phometric parameters: carapace length, vored during matings. 2) Do different pop- maximum carapace width, maximum car- ulations of H. tectifera display variation in apace height, maximum plastron length, body size and other biometric measure- maximum plastron width and posterior ments? We expect individuals from higher lobe width using a vernier caliper (see latitudes (southern populations) to be larg- Bager et al., 2016 for morphometric er than individuals of the lower ones in all measures details). The sex of adults was biometric measures. established by external examination of secondary sexual characteristics. Males Materials and methods usually have a longer and thicker tail than Study area females and male’s plastron is concave. We treated as juveniles those individuals We sampled turtle populations across in which sex could not be determined (CL two states in Brazil: Minas Gerais and Rio < 145 mm in MG and CL < 119 mm in RS), Grande do Sul (hereafter referred to MG but were not considered in this study due and RS), comprising four municipalities, to low sample size. Capture point of each between 1995 and 2011 (Table 1). In MG individual was recorded using GPS, all state sampling occurred in the Lavras mu- turtles were marked by notching the mar- nicipality, Campo das Vertentes Mesore- ginal scutes (Cagle, 1939) and then re- gion, a transitional area between Cerrado leased near the capture spot. and Atlantic Forest biomes, two Brazilian Data analysis hotspots of biodiversity (Myers et al., 2000; Mittermeier et al., 2004). The climate is Only measurements taken during the Cwa, with dry winters and rainy sum- first capture were used in the analyses. mers, and the average annual temperature Adults were grouped by sex and state of is 20.4°C (Dantas et al., 2007). Aquatic en- origin: MG males, MG females, RS males vironments in this region were composed and RS females. Morphometric variation mainly by swampy areas. In RS state sam- within Rio Grande do Sul populations 49 DA SILVA LUCAS ET AL. Table 1: Sampling areas (SA) of Hydromedusa tectifera with sampling interval (SI). State SA Latitude (S) Longitude (W) SI Minas Gerais (MG) Lavras 21°19ʹ45ʹʹ 44°58ʹ18ʹʹ 2010/2011 Arroio Grande 33°14ʹ21ʹʹ 53°08ʹ12ʹʹ 2000 Rio Grande do Sul (RS) ESEC Taim 32°32ʹ51ʹʹ 52°32ʹ40ʹʹ 1995/96/98/00/02/06 Pelotas 31°26ʹ11ʹʹ 56°22ʹ01ʹʹ 2001/02/03/06 were computed with an one-way ANOVA to identify the variables that most influ- to test the hypothesis that morphometrics enced this separation (Zuur et al., 2007). do not vary with close proximity. Normal Analyses were done using R (R Develop- distribution (Shapiro-Wilk test) and homo- ment Core Team 2015) and Bioestat (Ayres geneity of variance (Levene test) assump- et al., 2007).