Ontogenetic variation of plastral spotting pattern in Phrynops hilarii (Testudines, Chelidae)

ONTOGENETIC VARIATION OF PLASTRAL SPOTTING PATTERN IN PHRYNOPS HILARII (TESTUDINES, CHELIDAE)

Mario R. Cabrera ^1,2 Sonia E. Colantonio ^1,2

ABSTRACT

The plastral spotting variation in the chelid turtle Phrynops hilarii (Duméril & Bibron, 1835) in relation to sex, size, and geographic procedence of individuals was analyzed. States for qualitative characters were analyzed using non-parametric tests. Quantitative characters (shell and scute measurements) were standardized for body size by linear regression against carapace length, and were subjected to principal components analysis and canonical discriminant function analysis. Results suggest that increased plastral spotting is a polymorphic ontogenetic trait in P. hilarii. Neither hatchlings nor juveniles have plastral pattern moderately or heavily pigmented. The simplest pattern, however, may persist without changes in some adults. There are no differences between sexes. The spatial distribution of the plastral pattern is not ordered latitudinally or longitudinally, showing no relationship with gradients of elevation, temperature, or precipitation. This pattern trait lacks of taxonomic significance. The morphometric analysis failed to reveal any character of diagnostic utility in the plastron to support the possibility that these patterns correspond to different sympatric taxa.

KEYWORDS. Reptilia, Chelidae, Phrynops, pattern variation, South America.

INTRODUCTION

From its original description by Duméril & Bibron (1835), and through subsequent redescriptions (Boulenger, 1889; Freiberg, 1970; Pritchard, 1979; Ernst & Barbour, 1989; Cei, 1993), no variation in amount and distribution of pigment in the plastron of the turtle Phrynops hilarii has been recognized. Likewise, from its reinstatement to species rank by Freiberg (1970), P. hilarii is regarded as a homogeneous taxon, with no subspecies (Freiberg, 1977; Iverson, 1992; Cei, 1993). The revision of herpetological collections in Argentina, Brazil, and Uruguay revealed the existence in this species of variation in its plastral spotting, which might profitably be studied. The objectives are to determine the extent of this variation, its taxonomic significance (if any), and to analyze its geographic distribution and variation.

MATERIAL AND METHODS

Individuals of P. hilarii from throughout the species range were assembled from the following herpetological collections (acronyms of the institutions and name of curators in parentheses): Departamento Zoología Vertebrados, Universidad de la República, Montevideo (DZVU, F. Achával); Museo Nacional de Historia Natural, Montevideo (MHNM, H. Osorio and A. Mones); Museu de Ciências Naturais, Fundação Zoobotânica do Rio Grande do Sul, Porto Alegre (MCNZ, M. Leitão de Araujo); Museu de Zoologia, Universidade de São Paulo (MZSP, P. Vanzolini and A. Ramos Costa); Fundación Miguel Lillo, San Miguel de Tucumán (FML, S. Kretzschmar and G. Scrocchi); Museo Argentino de Ciencias Naturales, Buenos Aires (MACN, it includes specimens formerly at Centro Nacional de Investigaciones Iológicas, CENAI, G. Carrizo); Vivario del Museo de Ciencias Naturales e Históricas del Instituto Ruiz de Montoya, Posadas (IARM, A. Martínez); Museo de Ciencias Naturales y Antropológicas, Paraná, Entre Ríos (MER, C. Ceruti); Museo Provincial de Ciencias Naturales, Santa Fe (MFA, C. Virasoro and E. Fioramonti); Córdoba Zoo (ZOOC, D. Villarreal).

Specimens examined. BRAZIL, Rio Grande do Sul: Santa Maria, Rio Vacacaí (MCNZ 3032); São Leopoldo (MCNZ 3641, 3642); Porto Alegre, Belém Novo (MCNZ 0797-0799, 2098), Delta do Jacuí, Ilha das Flores (MCNZ 6545), Ilha do Cipriano (MCNZ 7124), Ilha do Lage (MCNZ 8177, 8618, 8758), Ilha dos Marinheiros (MCNZ 8416); Viamão, Passo do Vigário (MCNZ 1115, 1173, 1174, 1204, 1225, 4959), Porto das Pombas (MCNZ 4958); Rio Guaíba (MCNZ 1254, 4957, 4961); Santo Antônio da Patrulha (MCNZ 6113); Tramandaí (MCNZ 4960); Palmares do Sul (MCNZ 6826); Cidreira (MCNZ 5091, 5092, 6546); Tapes, Lagoa Formosa (MCNZ 6320); São Lourenço do Sul (MCNZ 6092); Rio Grande, Taim (MCNZ 6261, 6262), Estação Ecológica do Taim (MCNZ 9114; MZSP 3056). ARGENTINA, Santiago del Estero: Alberdi, Campo Gallo (MFA 10, 11); Chaco: San Fernando, Barranqueras (MZSP 2677, 2679); Misiones: Candelaria, Estancia San Juan Pirahui, between road 12 and Loreto (MACN 35398); Provincia de Misiones (IARM w/Nº, four live specimens); Corrientes: Saladas (MACN 35396); Alrededores de Goya (FML 00028); Santa Fe: Villano, Chacoan zone (MACN 7011); 10 km S El Carril (MACN 30489); between San José del Rincón and Río Colastiné (MACN 34819); Santa Fe (MACN 7080; MFA 15); Rosario (MACN [ex CENAI 16]); Córdoba: Cruz del Eje, Embalse de Cruz del Eje (AC 265); Río Suquía (ZOOC w/Nº, alive); Entre Ríos: La Paz, 3 km N Piedras Blancas (MACN 30472); Paraná (MACN 30486; MER 178, 180); "Río Paraná" (MER 176, 191); Departamento Paraná (MER 189); Diamante (MER 194); Crespo (MACN 20547, 35397); Departamento Tala (MER 3861); Gualeguaychú, 5 km W Ceibas, Estancia La Peregrina (MACN 35399); Buenos Aires: Pilar, Zelaya (MACN 10805). URUGUAY, Artigas: Río Cuareim, Sepulturas, Picada del Negro Muerto (DZVU 863); Río Cuareim, 32 km NW Artigas, Estancia Yuquerí (DZVU 2315, 2343); Arroyo Cuaró, Paso Campamento, Estancia La Escondida (MHNM 01390); Arroyo Catalán Chico (DZVU 635, 2340); near to arroyo Catalán Chico, Estancia Chilo Martínez (DZVU 295); Salto: Río Arapey Grande, 4 km W Las Termas (DZVU 2341); Paysandú: Paysandú (MACN 34516, 34517); Río Uruguay, Paso de Vera, in front of Almirón (DZVU 2423); Tacuarembó: Río Negro, Paso de los Toros (MHNM 01386); Valle Edén (DZVU 728); Cerro Largo: Río Tacuarí, Picada de Medina (MHNM 01629); Río Negro: Near Estación Francia (MHNM 02568); Río Negro, 15 km SSE Nuevo Berlín (DZVU 742); Costa del río Negro, in front of Villa Soriano (DZVU 762-765, 775-777); Lagoon 4 km from río Negro, in front of Villa Soriano (DZVU 783-785); Rocha: Río Cebollatí, Picada de Techera (DZVU 370); Soriano: Arroyo del Perdido (DZVU 2309; MHNM 01388); Estancia Santa Elena (MHNM 01391).

The samples totalled 96 turtles of both sexes and unsexed juveniles, ranging from 31 mm to 380 mm carapace length, and included whole fluid-preserved or dry animals, single carapaces, and living specimens.

States for the following qualitative characters were recorded for each turtle. (1) Plastral pattern (PP states, fig. 1). Three states defined as: (state a) plastron surface yellowish, with dark marks (usually a symmetrical pattern of black spots) arranged in two concentric series roughly complete; (state b) marks as in (a), but with small black dots irregularly dispersed; (state c) profuse irregular black marks throughout the plastral surface, usually masking the symmetrical pattern; (2) edge of carapace yellowish from dorsal view; (3) number and relative size of spots in both the lower surface of marginals and bridge.

In order to analyze geographic variation, the range of natural distribution of the species (excluding the anthropochoric records cited by Cabrera, 1998) was divided into five areas (A-E, fig. 2) each of them related to a major hydrographic basin: A) Paraná and Paraguay Rivers basin; B) Uruguay River basin; C) river systems draining mainly to the east, tributaries of the Mirim and dos Patos lagoons; D) and E) endorheic basins in the Argentine political provinces of Santiago del Estero and Córdoba, respectively. Areas D and E (fig. 2) were later excluded from further analysis due to insufficient data availability. Qualitative characters were analyzed using non-parametric (Contingency Coefficient, and Kruskal-Wallis) tests (Vanzolini, 1993).

Morphometric analysis were performed in order to analyze the potential relationship between PP states and measurable shell features. Shell measurements (to the nearest mm) and scute measurements (to the nearest 0.5 mm) were taken on each specimen with carapace length ³180 mm. From individuals smaller than this size only the carapace length and plastral pattern were recorded; because their shell outline and ratios differed markedly from those of adults, they were not included in the morphometric analyses.

Measurements, all straightline, included: maximum carapace length (CL); maximum plastron length (PL); midline length of plastron (MPL); midline length of the nuchal scute (NL); maximum length of the intergular scute (IL), and lengths of right interhumeral (IH), interpectoral (IP), interabdominal (IAb), interfemoral (IF), and interanal (IA) seams. Width measurements (straightline) included: maximum carapace width (CW); maximum width of first vertebral scute (V1); maximum width of fifth vertebral scute (V5); maximum width of plastral forelobe (PF); plastral forelobe width at the level of its base (PFB); width of the free edge of intergular scute (IW); maximum width of plastral hindlobe (PH); plastral hindlobe width at the level of its base (PHB).

These characters were standardized for body size by linear regression against CL, and the residuals were used in the statistical calculations. Arguments for the use of residuals as input variables were noted in Cabrera & Colantonio (1997) and references therein. The residuals were then subjected to ANOVA and MANOVA tests, principal components analysis (PCA) of the character correlation matrix, and canonical discriminant function analysis (DFA), using the SPSS (Statistical Package for Social Sciences) software version 5.0.1.

RESULTS AND DISCUSSION

Qualitative characters analysis. The following characters were independent of geographic procedence in Phrynops hilarii: a yellow rim around the carapacial margin, although some more marked in juveniles, was always visible dorsally; number and relative size of dark spots on both the plastral aspect of the marginal scutes and the bridge always showed a direct relationship to the abundance and size of the plastral spots. Consequently, these characters were not analyzed further.

All individuals adscribed well to one of the three alternative states of plastral pattern (PP). Although intermediate stages are expectable as a hatchling with state a grows into an adult with state b or c, the transition is perhaps relatively rapid; we consequently used PP states as comparative categories. In adults the relationship between sex and PP state was not significant (Contingency Coefficient C = 0.192, P = 0.316), suggesting independence between sex and PP states (tab. I). When PP was analyzed in relation to size we found that hatchlings and juveniles with CL up to 170 mm showed only the PP state a (fig. 3). The PP state c was only present in large individuals, in the samples examined those over 270 mm CL (except for one specimen with CL = 225 mm). The relationship between CL as an index of overall body size (and for extension, relative age), and the PP states was significant (Kruskal-Wallis H = 33.85, df = 2, P<0.001), with larger animals having more spotting.

The relationship among geographic areas A-C and PP states was not significant (C = 0.227, P = 0.357) (tab. II). The variation in plastral pattern was not clinal. There are localities where any two patterns were present (a and c states in Crespo, Entre Ríos; a and b states in Arroyo Catalán Chico, Artigas Department; b and c states in Estação Ecológica do Taim, Rio Grande do Sul). Moreover, geographic proximity and/or presence in the same major river basin of specimens showing any third state warrants the co-occurrence of the three states in many cases. The absence of the c state in area B is interpreted as a sampling artifact. The spatial distribution of the plastral patterns were not ordered latitudinally or longitudinally, showing no relationship with gradients of elevation, temperature, or precipitation.

Morphometric analysis. Residuals of four characters (IW, PHB, PL, and MPL) showed no univariate homogeneity of variance to Cochrans C and Bartlett-Box F tests, and were excluded from multivariate analysis of variance. Multivariate differences among PP states were not significant (Pillais F = 0.63105, df = 26, P = 0.235; Hotellings F = 1.04105, df = 26, P = 0.181; Wilks F = 0.45016, df = 26, P = 0.206). Only the character IAb showed significant differences among PP states (F = 7.456, P = 0.002).

The PCA results showed no clear separation among the PP states (fig. 4). Six principal components whose eigenvalues were higher than one were obtained (tab. III). The first principal component (PC1) accounted for 30.5% of the total variation. Characters more influential to PC1 were PF, PFB, PH, and PHB. The second principal component (PC2) accounted for 13.5% of the remaining variation. The most influential character was IH. The third principal component (PC3) accounted for 9.9% of the remaining variation. Characters most influential loading on PC3 were PL and MPL. Fourth to sixth components (PC4 to PC6) accounted for low percentages of the remaining variation (tab. III).

The DFA was congruent with the PCA showing that a clear separation among PP states was not evident (fig. 5). The percentage of cases correctly classified in its actual group was only 50% (tab. IV). The only canonical discriminant function explained 100% of the variability among PP states (Eigenvalue = 0.32, df = 2, P = 0.002), and was represented by the IAb character.

The morphometric analysis failed to reveal any character, or combination of them, of some diagnostic utility to support the possibility that these patterns correspond to different sympatric taxa. The only character statistically significant to ANOVA was the length of interabdominal seam, in agreement with the discriminant function obtained. However, this character as well as other midseam scute lengths with which the plastral formula is calculated, is variable in this species (Ernst & Barbour, 1989) as well as in turtles in general (Lovich & Ernst, 1989). These latter authors showed for seven families of chelonians that plastral formulae may differ between sexes and among size classes in a given taxon. Therefore, the use of these proportions as key characters to characterize individual species must be cautiously applied.

Results suggest that increased plastral spotting in P. hilarii is a polymorphic ontogenetic trait. Neither hatchlings nor juveniles ever have plastral pattern moderately or heavily pigmented (the states b and c). However, the simplest pattern (the a state), that is found in all of the specimens under 17 cm carapace length, persists without changes in some adults up to, at least, 38 cm of carapace length.

Results also show that this trait lacks of taxonomic significance. Notwithstanding, the description of plastral coloration of P. hilarii as referred hitherto by most authors is incomplete, and should be expanded to the following. Plastron pale yellow with black or dark brown spots. The pattern in hatchlings and juveniles up to 17 cm of carapace length is formed by two concentric series of circular or eliptical blotches, roughly symmetrically arranged, on most or all of the scutes. This pattern may persist unchanged into adulthood, even in very large individuals, or may be replaced by one of these variants: (a) a pattern showing spotting similar to that previously described accompanied by dots more or less abundant randomly dispersed on the scutes, or (b) a pattern formed by dark irregular and abundant spots all over the plastral surface, without persistence of the juvenil symmetric pattern. On the inframarginal and bridge surfaces the pattern corresponds to that of the plastron itself.

Acknowledgments. To the curators and authorities of the institutions for permitting free access to their collections, and for logistic support. To Peter C. H. Pritchard and one anonymous reviewer for their comments on earlier versions of the ms. To Gladys Sala for drawing the map. This research was supported by CONICOR (formerly Consejo de Investigaciones Científicas y Tecnológicas de la Provincia de Córdoba) grant 3971/97, and by SECYT-UNC (Secretaría de Ciencia y Tecnología de la Universidad Nacional de Córdoba, Argentina).

REFERENCES

Recebido em 31.08.2000; aceito em 11.07.2001

2. CONICET Researchers.

• Boulenger, G. A. 1889. Catalogue of the chelonians, rhynchocephalians, and crocodiles in the British Museum (Natural History). London, Taylor & Francis. 311 p.
• Cabrera, M. R. 1998. Las Tortugas continentales de Sudamérica Austral. Córdoba, Privately. 108 p.
• Cabrera, M. R. & Colantonio, S. E. 1997. Taxonomic revision of the South American subspecies of the turtle Kinosternon scorpioides J. Herpetol., Athens, 31:507-513.
• Cei, J. M. 1993. Reptiles del noroeste, nordeste y este de la Argentina. Mus. Reg. Sci. Nat. Torino, Turin, Monogr., 14:1-949.
• Duméril, A. M. C. & Bibron, G. 1835. Erpétologie générale ou histoire naturelle complète des Reptiles, 2. Paris, Roret. 680 p.
• Ernst, C. H. & Barbour, R. W. 1989. Turtles of the world Washington, DC, Smithsonian Institution. 313 p.
• Freiberg, M. A. 1970. Validez específica de Phrynops hilarii (D. et B.) (Testudines, Chelidae). Revta Mus. argent. Cienc. nat. Bernardino Rivadavia, Zool., Buenos Aires, 10:189-197.
• ___. 1977. Reptilia. Testudines o Chelonia. In: Ringuelet, R.A. Dir. Fauna de agua dulce de la República Argentina, Buenos Aires. v. 42, fasc.1, 55 p.
• Iverson, J. B. 1992. A revised checklist with distribution maps of the turtles of the world. Richmond, Privately. 363 p.
• Lovich, J. E. & Ernst, C. H. 1989. Variation in the plastral formulae of selected turtles with comments on taxonomic utility. Copeia, Washington DC, 1989:304-318.
• Pritchard, P. C. H. 1979. Encyclopedia of turtles New Jersey, T.F.H. Publications. 895 p.
• Vanzolini, P. E. 1993. Métodos estatísticos elementares em Sistemática zoológica São Paulo, HUCITEC. 130 p.

Publication Dates

• Publication in this collection
  15 July 2003
• Date of issue
  Nov 2001

History

• Accepted
  11 July 2001
• Received
  31 Aug 2000