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Morphology of the Shell of Happiella Cf. Insularis (Gastropoda: Heterobranchia: Systrophiidae) from Three Forest Areas on Ilha Grande, Southeast Brazil

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Morphology of the Shell of Happiella Cf. Insularis (Gastropoda: Heterobranchia: Systrophiidae) from Three Forest Areas on Ilha Grande, Southeast Brazil ZOOLOGIA 31 (3): 230–238, June, 2014 http://dx.doi.org/10.1590/S1984-46702014000300004 Morphology of the shell of Happiella cf. insularis (Gastropoda: Heterobranchia: Systrophiidae) from three forest areas on Ilha Grande, Southeast Brazil Amilcar Brum Barbosa1 & Sonia Barbosa dos Santos1,2 1 Laboratório de Malacologia Límnica e Terrestre, Departamento de Zoologia, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro. Rua São Francisco Xavier 524, PHLC sala 525-2, 20550-900 Rio de Janeiro, RJ, Brazil. 2 Corresponding author. E-mail: [email protected] ABSTRACT. We conducted a study on shell morphology variation among three populations of Happiella cf. insularis (Boëttger, 1889) inhabiting different areas (Jararaca, Caxadaço, and Parnaioca trails) at Vila Dois Rios, Ilha Grande, Angra dos Reis, state of Rio de Janeiro, Brazil. Linear and angular measurements, shell indices representing shell shape, and whorl counts were obtained from images drawn using a stereomicroscope coupled with a camera lucida. The statistical analysis based on ANOVA (followed by Bonferroni’s test), Pearson’s correlation matrix, and discriminant analysis enabled discrimination among the populations studied. The variable that most contributed to discriminate among groups was shell height. Mean shell height was greatest for specimens collected from Jararaca, probably reflecting the better conservation status of that area. Good conservation is associated with enhanced shell growth. Mean measure- ments were smallest for specimens from Parnaioca, the most disturbed area surveyed. Mean aperture height was smallest for specimens from Parnaioca, which may represent a strategy to prevent excessive water loss. Discriminant analysis revealed that the snails from Jararaca differ the most from snails collected in the two other areas, reflecting the different conservation status of these areas: shells reach larger sizes in the localities where the humidity is higher. The similarities in shell morphology were greater between areas that are more similar environmentally (Caxadaço and Parnaioca), suggesting that conchological differences may correspond to adaptations to the environment. KEY WORDS. Conchology; discriminant analysis; ecology; morphometry; threatened biome. Land snails are exceptionally diverse in morphology, for ombrophilous dense forest, now at different levels of regen- instance they display great polymorphism in shell color and eration (ALHO et al. 2002, OLIVEIRA 2002, ALVES et al. 2005, CALLADO variations in shell dimensions. For this reason, they are a good et al. 2009) from disturbances caused by a range of human ac- subject for evolutionary biology studies (CLARKE et al. 1978). tivities over the past five decades, being now a natural labora- Differences in size, morphology and growth rates are associ- tory to study shell morphological differentiation induced by ated with ecological conditions, natural selection, and phylo- in environment conditions. genetic history (VERMEIJ 1971, CLARKE et al. 1978, EMBERTON 1994, The focus of this study was to investigate variations in 1995b, COOK 1997, PARMAKELIS et al. 2003, TESHIMA et al. 2003). the morphology of the shell of Happiella cf. insularis in three According to GOULD (1984), the low mobility of land snails in- different environments (Table I). This species was described by fluences character variability. The literature shows that habi- BOËTTGER (1889) based on a single shell collected from the type tat alterations, which result in fragmentation, are an important locality, Ilha das Flores, São Gonçalo city, Rio de Janeiro, where factor affecting shell morphological differentiation (COOK 1997, additional specimens have not been found (SANTOS et al. 2010). GOODFRIEND 1986, EMBERTON 1982, 1994), which can be acceler- BOËTTGER’s (1889) description, which was not accompanied by ated in degraded environments (CHIBA 2004, CHIBA & DAVISON illustrations, highlighted the following diagnostic features: 2007). maximum diameter with 5.25 mm, shell height 2 mm, large Ilha Grande, a continental island in the southern por- umbilicus, one-fourth the size of the shell base; shell pebble- tion of the state of Rio de Janeiro, harbors large, continuous shaped, thin, white, polished, spire apex slightly prominent, and conserved fragments of Atlantic Forest (ROCHA et al. 2006), with ½ whorls, slightly convex; borders distinct, mildly stri- which is among the most threatened biomes in the world (MYERS ated, last border over the third, approximately as wide as shell, et al. 2000). Over 50% of Ilha Grande is covered by less arched at top than bottom, angled below central region; 2014 Sociedade Brasileira de Zoologia | www.sbzoologia.org.br | www.scielo.br/zool All content of the journal, except where identified, is licensed under a Creative Commons attribution-type BY-NC. Morphology of the shell of Happiella cf. insularis from three forest areas 231 suture deeply impressed. Aperture elliptical-lunular, with small slit, aperture height with 2 mm, aperture width with 2.25 mm, simple peristomatic edge, with curved, spherical, sub-angular syphunculus [sic] protruding to right side of base. THIELE (1927), in addition to the type locality of H. cf. insularis, also listed it in Piracicaba (state of São Paulo), Blumenau (state of Santa Catarina) and Porto Alegre (state of Rio Grande do Sul); MORRETES (1949) also listed it only in Ilha das Flores and SIMONE (2007) to Xanxerê and São Carlos (state of Santa Catarina). In the present study, we analyzed the shell morphology of three populations of H. cf. insularis subjected to different environmental conditions, with the goal to assess variability in shell morphology, as detailed morphology and range of varia- Figure 1. Location of Ilha Grande, in Angra dos Reis Municipality, tion can prove useful for refining species diagnoses. state of Rio de Janeiro, Brazil, showing the Jararaca, Parnaioca, and Caxadaço trails. Map: Luiz E.M. Lacerda. MATERIAL AND METHODS The specimens used in this study were collected from UERJ 1155); 30.XI.1997, D.P. Monteiro leg. (Col. Mol. UERJ three areas, known as the Jararaca, Caxadaço, and Parnaioca 1168-1 and 2); ditto, 26.VI.1999, S.B. Santos leg. (Col. Mol. UERJ trails, located in Vila Dois Rios, on the ocean side of Ilha 1241-1 and 2); 21.III.1997, S.B. Santos leg. (Col. Mol. UERJ 1252- Grande, Municipality of Angra dos Reis, southern region of 2); 14.I.1998, D.P. Monteiro leg. (Col. Mol. UERJ 1617-2); the state of Rio de Janeiro (23°04’25” to 23°13’10"S, 44°05’35” 17.II.1998, A.S. Alencar leg. (Col. Mol. UERJ 1618-2); 17.II.1998, to 44°22’50”W). In each collecting site (Fig. 1), a distinct level D.P. Monteiro leg. (Col. Mol. UERJ 1646); 15.I.1998, S.B. Santos of forest regeneration (VERA-Y-CONDE & ROCHA 2006) can be leg. (Col. Mol. UERJ 1647-2); 17.II.1998, M.A. Fernandez leg. found, making them suitable for investigations on the influ- (Col. Mol. UERJ 1650); 14.I.1998, A.S. Alencar leg. (Col. Mol. ence of environmental factors on shell morphology. UERJ 1651); 14.I.1998, D.P. Monteiro leg. (Col. Mol. UERJ 1653- Table I contains a summary of the environmental pa- 2); 17.I.1998, S.B. Santos leg. (Col. Mol. UERJ 1656-2 and 3); rameters measured at the three areas studied. 17.II.1998, D.P. Monteiro leg. (Col. Mol. UERJ 1658-2, 3, 4 and We selected intact shells from 102 adults, grown to ap- 6); 17.II.1998, S.B. Santos leg. (Col. Mol. UERJ 1659-1, 2, and proximately three whorls and proportionally similar to each 3). Vila Dois Rios, Trilha do Caxadaço, 19.X.1995, V.C. Queiroz other. Thirty-three shells from the Jararaca Trail were selected, leg. (Col. Mol. UERJ 999-2, 3, 4, 5, and 6); 30.V.1997, S.B. Santos in addition to 34 and 35 shells from the Caxadaço and leg. (Col. Mol. UERJ 1064-7 and 3); 28.XI.1997, D.P. Monteiro Parnaioca trails, respectively. leg. (Col. Mol. UERJ 1110-1, 2, 3, 4, and 5); 15.VIII.1996, S.B. Material examined. Happiella cf. insularis. BRAZIL, Rio de Santos leg. (Col. Mol. UERJ 1114); 19.X.1995, V.C. Queiroz leg. Janeiro: Angra dos Reis, Ilha Grande, Vila Dois Rios, Trilha da (Col. Mol. UERJ 1144-1, 2, 3, and 4); 08.VIII.1999, M. Sttorti Jararaca, 14.VI.1998, S.B. Santos leg. (Col. Mol. UERJ 942-1); leg. (Col. Mol. UERJ 1310); 21.X.2000, D.P. Monteiro leg. (Col. 27.IX.1996, S.B. Santos leg. (Col. Mol. UERJ 977); 11.I.1996, Mol. UERJ 2061-1, 2, and 3); 15.III.2001, S.B. Santos leg. (Col. V.C. Queiroz leg. (Col. Mol. UERJ 980-4 and 5); 12.I.1996, S.B. Mol. UERJ 2156-2, 3, 4, 5, and 6); 28.X.2001, C.C. Siqueira leg. Santos leg. (Col. Mol. UERJ 990-1 and 2); 21.III.1997, S.B. Santos (Col. Mol. UERJ 2225-2, 3, 4, 5, and 6); 2.VIII.2005, A.B Barbosa, leg. (Col. Mol. UERJ 1132); 23.III.1997, S.B. Santos leg. (Col. Lacerda, L.E.M., T.A. Viana leg. (Col. Mol. UERJ 7445-1, 2, and Mol. UERJ 1133-1 and 2); 20.IX.1997, S.B. Santos leg. (Col. Mol. 3). Vila Dois Rios, Trilha da Parnaioca), 28.V.1997, N. Salgado Table I. Summary of local environmental parameters from three areas (Jararaca, Caxadaço and Parnaioca trails) at Ilha Grande. Mean ambient Mean ground Mean leaf litter Mean relative Canopy Canopy Time of Area temperature temperature depth layer (a) air humidity Elevation Degree of impact height (m) closure regeneration (a) (°C) (a) (°C) (cm) (a) (%) Jararaca Trail 22.46 ± 3.42 20.81 ± 3.42 7.17 ± 2.68 84.81 ± 9.27 33 (c) Greater 250 m asl Advanced stage of At least 90 ecological succession years-old (e) Caxadaço Trail 29.95 ± 2.09 21.01 ± 2.15 4.11 ± 1.64 83.82 ± 8.98 15-20 (b) Intermediate 180 m asl Early stage of At least 50 ecological succession years-old (c) Parnaioca Trail 25.29 ± 3.12 22.04 ± 2.16 5.87 ± 2.66 80.93 ± 10.51 15 (c) Lower At sea level Early stage of 5 to 25 ecological succession years-old (c) a) D.P.
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