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Color Variation Among Habitat Types in the Spiny Softshell Turtles (Trionychidae: Apalone) of Cuatrocie´Negas, Coahuila, Mexico

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Color Variation Among Habitat Types in the Spiny Softshell Turtles (Trionychidae: Apalone) of Cuatrocie´Negas, Coahuila, Mexico Journal of Herpetology, Vol. 42, No. 2, pp. 347–353, 2008 Copyright 2008 Society for the Study of Amphibians and Reptiles Color Variation among Habitat Types in the Spiny Softshell Turtles (Trionychidae: Apalone) of Cuatrocie´negas, Coahuila, Mexico SUZANNE E. MCGAUGH Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, Iowa 50011, USA; E-mail: [email protected] ABSTRACT.—Ground coloration is highly variable in many reptile species. In turtles, ground color may correspond well to the background coloration of the environment and can change over time to match new surroundings in the laboratory. Variable carapace and plastron coloration across three habitat types were investigated in the Black Softshell Turtle, Apalone spinifera atra, by measuring individual components of the RGB (Red, Green, Blue) color system. In general, A. s. atra carapaces were darker in turtles from lagoons than in turtles from playa lakes. Red and green values were significantly different among all pairs of habitat types, but blue values differed only between the playa lakes and lagoons. Mean color components (RG only) for each population were significantly correlated with corresponding values for the bottom substrate, indicating a positive association of carapace and habitat substrate color components. In contrast, plastron ground color RGB channels showed no significant differences between habitat types and no significant correlations with substrate RGB. These results suggest that dorsal background matching in A. s. atra may be responsible for some of the variation in this key taxonomic trait. The color of an organism is an important spinifera emoryi (Winokur, 1968), but adults component of many aspects of an organism’s show marked differences in coloration across biology and is often used as a taxonomic habitats (this study), which could be a result character (Endler, 1990; Brodie and Janzen, of genetically based ontogenetic pigmenta- 1995; Darst and Cummings, 2006). Yet, an tion variation among habitats or phenotypic animal’s coloration may be plastic and can plasticity in response to substrate color varia- depend on many different biotic and abiotic tion. factors (Endler, 1990; Bennett et al., 1994). For Apalone spinifera atra was originally described example, overall habitat irradiance is a common as an isolated species (Webb and Legler, 1960), stimulus for physiological color change in but canal building in the late 1800s was thought reptiles, presumably as a means to become to have opened the basin hydrologically, result- more cryptic (Norris and Lowe, 1964; Rosen- ing in opportunities for hybridization between blum, 2005; Rowe et al., 2006a). This physiolog- A. s. atra and A. s. emoryi (Smith and Smith, ical response occurs rapidly and uses hormonal 1979; Ernst and Barbour, 1992). A recent genetic signals to expand or contract melanophores in evaluation found no differentiation between the dermal layer of skin (Bartley, 1971). Inter- morphologically identified A. s. atra individuals estingly, laboratory tests indicate that the shells and morphologically identified A. s. emoryi and skin of turtles, too, can change color to individuals within and outside the basin more closely match dark or light backgrounds, (McGaugh and Janzen, in press). However, although this change occurs over weeks or substantial coloration differences exist among months (Woolley, 1957; Bartley, 1971; Rowe et habitats and this phenotypic variation was left al., 2006b). unexplained by the genetic study. Examination Cuatrocie´negas in Coahuila, Mexico, offers a of the color variation of the softshell turtles unique ecosystem in which to observe natural across the basin, in relation to background variation in shell color of turtles across three coloration of habitats (Woolley, 1957; Bartley, very different aquatic habitat types (Winokur, 1971; Rowe et al., 2006b), may provide an 1968). The region’s endemic and endangered important morphological perspective on A. s. Softshell Turtle, Apalone spinifera atra (atra atra’s refuted species delimitation (McGaugh meaning black or dark; Webb and Legler, and Janzen, in press). For simplicity, and 1960; Lovich et al., 1990, Fritz and Havasˇ, because haplotypes in the genetic study showed 2006), is taxonomically defined by its dark no morphological (i.e., light and dark turtles pigmentation, and the validity of A. s. atra as a shared mitochondrial and nuclear DNA haplo- full species has been challenged (Smith and types) or geographic grouping, the name A. s. Smith, 1979). Hatchlings of A. s. atra cannot be atra is used to refer to all Apalone in this study, differentiated from a lighter conspecific, Apalone even though A. s. emoryi morphs are present in 348 S. E. MCGAUGH the basin (Smith and Smith, 1979; McGaugh and (Evans, 2005) and spanned 30 days of trapping Janzen, in press). (4 June to 5 July 2004). In this study, I evaluated the hypothesis that Turtles were captured in lobster or hoop background matching could be responsible for traps baited with sardines. Each A. s. atra was the observed color variation across habitats in tattooed with a unique pattern on the plastron. A. s. atra. To evaluate this hypothesis, coloration Plastron length was measured with dial calipers of the animals’ carapace and plastron and to the nearest millimeter, and sex was deter- locality substrate was measured. Background mined by tail length (Webb and Legler, 1960), matching was expected to be probable if with males identified by a much longer tail than carapace, but not plastron coloration, was females relative to their body size. All A. s. atra correlated to locality substrate coloration. had plastron lengths over 73 mm. Hatchling Color was measured with digital photographs and juvenile turtles were not included in the using the RGB system (red, green, blue; Stevens analysis. Sixty total individuals were sampled et al., 2007), the components of which corre- (Lagoon1: N 5 16, Lagoon2: N 5 6, Lagoon3: N spond to broad bands of longwave (red), 5 13, River: N 5 10, Playa lake1: N 5 10, Playa mediumwave (green), and shortwave (blue) lake2: N 5 5). light (Stevens et al., 2007). Possible influences Digital Photography and Analysis.—Digital of sex, size, and their interactions were also photographs were taken with a Canon Power evaluated. Shot G5 that was positioned directly above the turtle. Color component measurements from MATERIALS AND METHODS digital systems have been shown to be positive- ly correlated with values from spectrometry, Study Site and Field Methodology.—Three main and digital photography has many advantages habitat types, playa lakes (barrial lakes), la- over spectrometry for data acquisition in the goons, and a river, were investigated within El field (Rowe et al., 2006a; Stevens et al., 2007). A A´ rea de Proteccio´n de Flora y Fauna Cuatrocie´- level on the tripod ensured that the camera lens negas, Coahuila, Mexico. This area of high was parallel to the ground. The lens-to-animal endemism contains diverse habitats, including distance measure was not taken. Photos were hundreds of small water bodies nestled within taken out of direct sunlight and with the flash the Chihuahuan desert (Minckley, 1969; Meyer, on and white balance off. Each photo was taken 1973). Playa lakes are large, shallow lakes with the highest resolution possible for the (,1 m deep) with sparse vegetation, large daily 3 temperature fluctuations, and relatively high camera (2,592 1,944 pixels) and converted to mineral content (Minckley, 1969). Lagoons are JPEG at the highest quality compression level typically deeper lakes (,1–10 m) with abundant available on the camera. vegetation, including waterlilies (Nymphaea), Digital quantification of color was performed muskgrass (Chara), pondweeds (Potamogeton), using Jasc Paint Shop Pro9 (Corel, Eden Prairie, and cattails (Typha), and relatively constant MN) by viewing the untransformed values of R, temperatures (Minckley, 1969). Rivers are flow- G, and B in the diagnostic histogram. The HSL ing channels with steep banks that are up to (Hue, Saturation, Lightness) system was not 2.5 ms deep and have vegetation such as used in the analysis because this system may be Nymphaea, Chara, Potamogeton, Typha, bladder- inaccurate (Stevens et al., 2007). In Jasc Paint worts (Utricularia), and sedge (Eleocharis) where Shop Pro9, the histogram displays a distribution the current is slow (Minckley, 1969). Most graph of the separate channels of color in an aquatic habitats in Cuatrocie´negas have clear image and allows the user to analyze the water with a visible bottom. distribution. A swath of at least 100 square Six localities were examined for A. s. atra, and pixels was selected from the right middle localities with the same habitat types (e.g., portion of the carapace and the plastron of A. lagoons) were combined in statistical analysis s. atra. All photos were analyzed at a resolution except for the Pearson’s correlation analysis of 70.866 pixels per cm. Therefore, each A. s. atra 2 (described below). All habitats used in this sample was $14 mm . Some A. s. atra had a study are stable bodies of water of unknown blotched pattern on their carapaces, and these geologic age. No aboveground aquatic connec- were included in the analysis. Otherwise, their tions are known between the localities used in pigmentation was generally uniform. Care was this study. Turtle dispersal between sites may taken during analysis only to sample areas with not be frequent because sites are separated by a clear view of the carapace (i.e., flash glares, distances (5.53–31.58 km) greater than other algae growth, mineral deposits, or bite marks on species of softshells typically travel terrestrially the animal were excluded from the swath). (Galois et al., 2002). Sampling for shell colora- Intraindividual color variability was not mea- tion included all five drainages of the basin sured because of these various obstructions. COLOR VARIATION IN APALONE 349 A grey color standard (paint swatch EE2054C Statistical Analysis.—To test for habitat struc- from Lowe’s Home Improvement Warehouse) turing in color components, data were trans- was placed in each photo.
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