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Morphometric Variation of Pipa Pipa (Linnaeus, 1758) (Anura: Pipidae) with Notes on Diet and Gonad Development

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Morphometric Variation of Pipa Pipa (Linnaeus, 1758) (Anura: Pipidae) with Notes on Diet and Gonad Development Herpetology Notes, volume 7: 347-353 (2014) (published online on 26 May 2014) Morphometric variation of Pipa pipa (Linnaeus, 1758) (Anura: Pipidae) with notes on diet and gonad development Helena Nery Alves-Pinto1, Vanessa Kruth Verdade2* and Miguel Trefaut Rodrigues1,3 Abstract. Pipa pipa is an emblematic and endemic aquatic frog from the Amazonian Basin, but much of its biology remains poorly known. In this paper we focused on morphometric variation, diet and gonad examination of P. pipa. We measured 23 morphometric variables in 56 individuals of P. pipa and tested for sexual dimorphism and for geographic variation using Principal Component Analysis. Data on diet and gonad development were studied in one population. The morphometric study showed that forearm diameter, finger and snout length are sexually dimorphic characteristics, all larger in males. The most abundant item found in the species’ diet was Cyclopoida, whereas Heteroptera represented the group with the highest occurrence in stomachs. Keywords: Pipidae; sexual dimorphism; diet; morphology; reproduction Introduction and behavioural characteristics (Trueb and Massemin 2000). The reproductive behaviour involves a turnover The frog family Pipidae occurs in Africa and America action, during which the couple swims in vertical circles and includes peculiar aquatic species (Canatella and in the water together while the eggs are released and laid Trueb, 1988; Duellman and Trueb, 1994; Frost et al., on the female back (Rabb and Rabb, 1960; Rabb and 2006). It is monophyletic and one of the most basal Snedigar, 1960; Rabb, 1961). Males are smaller than anuran groups (Canatella and Trueb, 1988; Frost et al., females and have thicker forearms (Zippel, 2006). The 2006, Irisarri et al. 2011). Among the four genera in the female’s vent is rounder and more turgid, especially family (Hymenochirus, Pipa, Pseudhymenochirus and during reproductive periods (Rabb and Snedigar, Xenopus), Pipa is the only genus occurring in Central 1960; Rabb, 1961; Zippel, 2006). However, no other and South America (Dunn, 1948; Canatella and Trueb, characteristics have been investigated regarding sexual 1988; Frost, 2011), from which four out of seven dimorphism and those listed are either subjective or species occur in Brazil - P. arrabali Izecksohn 1976, observed only during reproductive periods. P. snethlageae Müller 1914, P. carvalhoi (Miranda- Aspects of the biology of Pipa pipa other than Ribeiro, 1937), and P. pipa (Trueb and Cannatella, amplexus behaviour have also been neglected and 1986). most information available comes mainly from captive Pipa pipa, the largest species in the genus (Dunn, individuals (Zippel, 2006). Literature on diet of the 1948; Rabb, 1961), has distinct external, osteological species recorded fish as well as anurans of genus Leptodactylus (Deckert, 1917; Duellman, 1978). During foraging, the species uses a combination of inertial suction and forelimb movements, and sometimes prey can be grasped between digits (Carreno and Nishikawa, 1 Universidade de São Paulo, Instituto de Biociências, 2010). Departamento de Zoologia, Rua do Matão, travessa 14, nº Reproductive biology and diet are relevant traits 10, Butantan 05422-970, São Paulo, SP, Brazil, e-mail: of natural history that affect survival, define habitats [email protected] and behaviours (Cuello et al., 2006). The lack of 2 Universidade Federal do ABC, Centro de Ciências Naturais e information on the ecology and biology of species is Humanas, Avenida dos Estados 5001, Bairro Bangu 09210- 580, Santo André, SP, Brazil usually the largest obstacle to management projects and 3 [email protected] conservation of anuran fauna (Greene, 2005; Silvano * Corresponding Author: [email protected] and Segalla, 2005; Verdade et al., 2012). The aim of 348 Helena Nery Alves-Pinto et al. this study was to identify sexual dimorphism from considering an imaginary mid-line between head and morphometric characteristics in the species Pipa pipa urostile; tibia length (TIL); eye diameter (ED); hand and geographical variation on morphometric variables length (HL); fingers 1 to 4 length (F1 – 4 L); foot length between populations. We also provide notes on its diet (FOL) (Verdade and Rodrigues 2007); mouth (Mt); and gonad development. forearm length (FL) (Márquez-Garcia et al. 2009); forearm diameter (FD) from dorsal to the ventral side Materials and Methods in an imaginary mid-line between elbow and hand; toes 1 to 5 length (T1 – 5 L) from base to the tip of each toe; We studied 61 individuals of Pipa pipa from three interdigital membranes 1 to 4 length (IM1 – 4 L) from different sources: individuals (n=32) collected in the base to the tip considering an imaginary mid-line January 2007 near the left bank of Abacaxis River, São between toes; and snout length (SL) from the tip of the Sebastião village, Borba municipality, Amazonas state, mid-line of the jaw to the tip of the snout. We measured Brazil (4º18’32” S, 58º 38’11” W) (MZUSP 142744– variables on the left side of all individuals, with a digital 775); individuals (n=4) collected in April 2010 at the calliper. right bank of Madeira river, Abunã village, Porto Velho To test sexual dimorphism we used variables’ residuals municipality, Rondônia state, Brazil (9º37’45” S, 65º from a regression analysis in order to avoid biases in 27’19” W) (MZUSP 143285–286, 144395–396); and morphometric comparisons. Levene’s and Shapiro Wilk individuals (n=25) from different localities, deposited at tests were performed to test normality and residual’s the Museu de Zoologia da Universidade de São Paulo variance. A One-way ANOVA was made with normal (MZUSP) collection (MZUSP 1006, 2036, 15903, and homogeneous data, whereas a Mann-Whitney U 16066, 16068, 23062, 23119, 23215, 23374–76, 23795, test was performed with the nonparametric residuals. 37519, 54799–800, 58534–35, 80450, 80454–55, We studied morphological geographic variation using 80474–78). all three samples: from São Sebastião, Abunã and The sample from São Sebastião village (Abacaxis previously specimen deposited at MZUSP, totalizing River) was assembled from a pond approximately six 61 individuals (one young excluded from the original meters long by six meters wide and 30 centimetres deep, sample) of Pipa pipa from 12 different localities. We in an area susceptible to seasonal flooding. The water performed Principal Component Analysis to explore was muddy, and leaf litter and mud covered the bottom. any group formation based on morphometric variation. The stream where individuals from Abunã village All variables listed earlier in this study were included were found was approximately one meter deep and in the analysis. Statistics was performed in SPSS 20.0 three meters wide, and had similar aspects as the São for Windows. Sebastião pond. All individuals were euthanized using a lethal dose of anaesthetic , preserved in 10% formalin Gonad development and stored in 70% ethanol. Gonadal studies were restricted to the sample of São Morphometric studies Sebastião, since we could not examine internal anatomy from the other populations. Testis length, diameter and We tested sexual dimorphism in 32 individuals from volume were measured and compared to male’s weight the São Sebastião sample, in which sex was determined and size using correlation analysis. Diameter, weight by gonad examination. The other samples were not and number of developed ova were measured. included in this analysis since gonad examination was not possible. Sexual maturity was determined based on Diet the snout-vent length (SVL) and gonad development. According to Schuette and Ehrl (1987), only individuals Dietary studies were also restricted to the sample of larger than 60 mm are considered adults. Although São Sebastião, since we could not remove stomach sexual maturity may vary from one population to contents from the other populations. The approximated the other, we still considered this size limit since all time between collection of animals and fixation was of individuals were larger than 60 mm with the exception one day. All individuals had their gastric and intestinal of one, a 36 mm juvenile. contents analysed under a stereoscope microscope. Prey Thirteen measurements were obtained and analysed length and diameter were measured, and prey category in this study: snout-vent length (SVL); body height identified to the level of Order. Degraded items were (BOH) taken from dorsal to the ventral side of the body not considered because they could not be identified. Morphometric variation of Pipa pipa with notes on diet and gonad development 349 Figure 1. Geographic distribution of Pipa pipa based on literature data (Vaz-Silva and Andrade 2009) and on our data. The frequency of appearance of each prey, as well as (p= 0.650, F=0.210), but forearm diameter (FD) (p=0.00 the occurrence of stomachs that contained each prey F=26.833), finger 2 length (p=0.00; F=12.522) and was determined. Prey volume was approximated to snout length (SL) (p=0.03, F=10.614) were significantly the ellipsoid volume, calculated based on the formula different between males and females. SL represented of a prolate spheroid V = 4/3π * L/2 * (W/2)2, where between 3.4 to 4.8% of SVL in females, while in males V=volume, L=length, and W=width. it ranged from 3.8 to 5.4% of SVL. To investigate the geographic variation in Results morphometric variables of Pipa pipa, data were taken from 12 localities (Figure 1), nine of which were not Morphometric studies registered by Vaz-Silva and Andrade (2009), who We found 17 males and 15 females in the São summarized the distribution of the species. Differences Sebastião sample. The One-way ANOVA showed that between groups did not clearly split populations. males and females do not differ on snout-vent length According to the Principal Component Analysis, the 350 Helena Nery Alves-Pinto et al. Figure 2. Plot of scores of the first and second components for the Principal Component Analysis, showing the geographic variation of different populations of Pipa pipa, based on morphological characters.
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