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Ontogenetic melanism in three populations of red-eared slider turtles (Trachemys scripta) in Oklahoma.

Ontogenetic melanism is characterized by an irreversible, progressive increase in pigmentation and is well documented in red-eared slider turtles (Trachemys scripta) and several other species of emydid turtles (Barbour and Carr, 1940; Lovich et al., 1990; Yabe, 1994; Seidel, 2003). In T. scripta, melanism typically is seen in adult males and first appears in the plastral scutes, followed by encroachment onto the carapace and soft tissue of the head, neck, and legs (McCoy, 1966). Onset of melanism in males coincides with the population-specific size of females at maturity (Thomas and Parker, 2000). Melanistic males tend to be older and larger than non-melanistic males within a population, but in T. scripta, melanism is not a direct factor of age. We compared incidence and average size of our melanistic males to melanistic T. scripta collected from the same population studied by McCoy (1966) at Lake Carl Blackwell, Payne Co., Oklahoma. We also made geographic comparisons among three populations of T. scripta in Oklahoma and between populations of T. scripta living in contaminated and non-contaminated habitats.

Tucker et al. (1995) divided progression of melanism in T. scripta into three stages. Stage 0 melanism is represented by turtles showing characteristic coloration with well-developed bars on costal scutes, bright yellow stripes on head and legs, and a red postorbital bar. Stage 2, full melanism, is characterized by a brown carapace with black borders along margins and completely obscured markings on head and leg. Turtles in stage 1 have coloration between stages 0 and 2. Turtles categorized in Stage 0 or 1 typically are classified as non-melanistic and those in stage 2 as melanistic. Tucker et al. (1995) reported that male T. scripta reach stage-2 melanism at 11-14 years of age and Lovich et al. (1990) reported estimates of 14.8 and 8.8 years for slow-growth and fast-growth populations, respectively.

We collected T. scripta from three sites in Oklahoma; Lake Carl Blackwell, Payne County; Sequoyah National Wildlife Refuge, Sequoyah, Haskell, and Muskogee counties; and Tar Creek Superfund Site, Ottawa County. Lake Carl Blackwell is a recreational lake owned by Oklahoma State University. Turtles were collected in Pine Grove Slough, an area closed to boat traffic, but connected to the main lake via a drainage system. At Sequoyah National Wildlife Refuge, turtles were collected from Little Vian Creek, which flows into Sally Jones Lake. Tar Creek Superfund Site was heavily mined for lead, zinc, and cadmium from the 1890s to the 1970s. Trachemys scripta was collected from Beaver Creek, which flows through the Catholic 40, a 17-ha portion of the site owned by the Quapaw Tribe of Oklahoma. No remediation or restoration efforts have been undertaken at the Catholic 40, and Beaver Creek floods over onto piles of mine tailings during periods of heavy rain. Ultimately, Beaver Creek drains into the Neosho River. The three sites exhibit moderate flow throughout most of the year and the surrounding vegetation is similar. The area surrounding Beaver Creek at Tar Creek Superfund Site is more disturbed than Lake Carl Blackwell and Sequoyah National Wildlife Refuge, but maintains aquatic and riparian plant communities.

All animals were handled following approved field methods (ACUP AS0315). Turtles were collected with hoop nets baited with sardines July-September 2003 and April-October 2004. Traps were set in early evening and checked each morning for a maximum of 48 h or until 20 animals were collected. Upon collection, animals were placed in a 62-L tub with 6-9 cm of local water. Animals were weighed with a Pesola spring scale and straight-line length and width of carapace and plastron were measured to the nearest 1 mm. Sex was determined by presence of secondary sex characteristics (Ernst et al., 1994). Animals were classified as melanistic (stage 2) or non-melanistic (stage 0 or 1). We gave each turtle a unique scute notch (Cagle, 1939) and released them at the point of capture.

At the three sites, 167 adult males (length of plastron >100 mm) were collected (Lake Carl Blackwell, n = 24; Sequoyah National Wildlife Refuge, n = 91; Tar Creek Superfund Site, n = 52). We categorized adult males into size classes based on length of plastron as presented by McCoy (1966): class A, 100-119 mm; class B, 120-139 mm; class C, 140-159 mm; class D, 160-179 mm; class E, 180-199 mm; class F, ?200 mm. We calculated frequency of melanistic and non-melanistic males in each size category (Fig. 1). The population at Lake Carl Blackwell had highest incidence of melanism in size classes D and E. Highest frequency of melanistic males from Sequoyah National Wildlife Refuge was in size class D and few animals in classes E and F were captured. However, Tar Creek Superfund Site had relatively low proportions of melanistic males among size classes C, D, and E. We used analysis of variance to compare mean size of melanistic males among collection sites and a significant difference (F = 14.86; df = 2; P < 0.001) was detected. Duncan's test for multiple comparisons indicated that mean length of plastron of melanistic males from Lake Carl Blackwell (178.1 mm) and Tar Creek Superfund Site (174.3 mm) were not significantly different at the 0.05 significance level; however, both Tar Creek Superfund Site and Lake Carl Blackwell were significantly larger than Sequoyah National Wildlife Refuge (163.4 mm). These results are consistent with Thomas and Parker (2000) who reported average length of plastron of melanistic males in Mississippi to be 178.1 and 175.4 mm. Average sizes of adult females at the three sites (Lake Carl Blackwell 196 mm; Sequoyah National Wildlife Refuge 183 mm; Tar Creek Superfund Site 198 mm) are consistent with the hypothesis that onset of melanism is related to population-specific size of females at maturity (Thomas and Parker, 2000). Tar Creek Superfund Site had the smallest minimum size of melanism at length of plastron = 114 mm and Sequoyah National Wildlife Refuge and Lake Carl Blackwell followed with 130 and 156 mm, respectively. Minima for Lake Carl Blackwell are similar to McCoy (1966) who presented minimum size of melanistic males from Lake Carl Blackwell as 145 mm. Minimum lengths of plastron of melanistic T. scripta from several studies are presented in Table 1. Percentage of males exhibiting melanism at each site was calculated and values compared using Chi-squared frequency tests. Of adult males, 75% at Lake Carl Blackwell, 60% at Sequoyah National Wildlife Refuge, and 44% at Tar Creek Superfund Site were melanistic. The proportion of melanistic males was significantly different among the three sites ([[chi square].sub.2] = 7.091, P = 0.029).

[FIGURE 1 OMITTED]

In reviewing life history of T. scripta, it becomes evident that attainment of melanism is not a geographic factor or a factor of size of male. Attainment of melanism is related rather to population-specific size of females at maturity. Results of assessment of three populations of T. scripta presented in this study fall within minimum sizes of melanism in previously published studies (Table 1). It is important to consider the role that heavy metal contamination at Tar Creek Superfund Site might play in attainment of melanism. Minimum size of attainment of melanism at Tar Creek Superfund Site falls well within the values reported in this and other studies suggesting that females in this population are maturing at a similar size to those in non-contaminated populations. However, the lower incidence of melanism at Tar Creek Superfund Site might indicate that fewer males are attaining the minimum size necessary to become melanistic or higher mortality is occurring in adult turtles at Tar Creek Superfund Site. Animals we collected from Lake Carl Blackwell had a larger size of attainment of melanism than previously reported by McCoy (1966), but this might be partially explained by collection methods used. McCoy obtained turtles from a hibernaculum in February, whereas turtles in our study were collected in hoop nets during the active season over the course of 10 months. Results presented in our study may provide a more accurate value of minimum size for attainment of melanism because of a broader sample of the population at Lake Carl Blackwell.

Associate Editor was William I. Lutterschmidt.

We thank Oklahoma State University, Quapaw Tribe of Oklahoma, and United States Fish and Wildlife Service for access, J. R. Bidwell, S. F. Fox, and P. Stone for comments on an early version of the manuscript, R. Torres-Cervantes for translation of the abstract, and Oklahoma State University Department of Zoology and Graduate College, Sigma Xi, Society of Environmental Toxicology and Chemistry, and EA Engineering for funding.

Submitted 29 August 2007. Accepted l May 2008.

LITERATURE CITED

BARBOUR, R. W., AND A. F. CARR, JR. 1940. Antillean terrapins. Memoirs of the Museum of Comparative Zoology at Harvard College 54:381-415.

CAGLE, F. R. 1939. A system of marking turtles for future identification. Copeia 1939:155-162.

CAHN, A. R 1937. The turtles of Illinois. Illinois Biological Monographs 16:1-218.

ERNST, C. H., J. E. LOVICH, AND R. W. BARBOUR. 1994. Turtles of the United States and Canada. Smithsonian Institution Press, Washington, D.C.

GARSTKA, W. R, W. E. COOPER, JR., K. W. WASMUND, AND J. E. LOVICH. 1991. Male sex steroids and hormonal control of male courtship behavior in the yellowbellied slider turtles, Trachemys scripta. Comparative Biochemistry and Physiology, Part A: Molecular and Integrative Physiology 98:271-280.

LOVICH, J. E., C. J. McCoy, AND W. R. GARSTKA. 1990. The development and significance of melanism in the slider turtle. Pages 233-256 in Life history and ecology of the slider turtle (J. W. Gibbons, editor). Smithsonian Institution Press, Washington, D.C.

McCoy, C. J. 1966. The development of melanism in an Oklahoma population of Chrysemys scripta elegans (Reptilia: Testudinidae). Proceedings of the Oklahoma Academy of Science 47:84-87.

SEIDEL, M. E. 2003. Trachemys decussata angusta. Herpetological Review 34:363-364.

THOMAS, R B., AND W. S. PARKER. 2000. Intersexual variations in overland movements of slider turtles (Trachemys scripta). Journal of Herpetology 34: 469-472.

TUCKER, J. K., R. J. MAHER, AND C. H. THEILING. 1995. Melanism in the red-eared slider (Trachemys scripta elegans). Journal of Herpetology 29:291-296.

WEBS, R. G. 1961. Observations on the life histories of turtles (genus Pseudomys and Groptemys) in Lake Texoma, Oklahoma. American Midland Naturalist 65:193-214.

YABE, T. 1994. Population structure and male melanism in Reeves' turtle, Chinemys reevesii. Japanese Journal of Herpetology 15:131-137.

KIMBERLY A. HAYS * AND KAREN MCBEE

Department of Zoology and Collection of Vertebrates, Oklahoma State University, 430 Life Sciences West, Stillwater, OK 74078

* Correspondent. kimberly.hays@okstate.edu
TABLE 1--Minimum size (length of plastron in mm)
at attainment of melanism in male Trachemys scripta.

 Size
Locality (mm) Reference

Texas 100 Cagle, 1950
South Carolina 104 Lovich et al., 1990
Tar Creek Superfund Site, Oklahoma 114 This study
Illinois and Tennessee 130 Cagle, 1950
Sequoyah National Wildlife Refuge, Oklahoma 130 This study
Alabama 140 Garstka, 1991
Lake Carl Blackwell, Oklahoma 145 McCoy, 1966
Illinois 152 Cahn, 1937
Lake Texoma, Oklahoma 152 Webb, 1961
Lake Carl Blackwell, Oklahoma 156 This study
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Title Annotation:NOTES
Author:Hays, Kimberly A.; McBee, Karen
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1USA
Date:Mar 1, 2009
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