Growth, Sexual Maturity, and Reproduction of a Female Midland Painted Turtle (Chrysemys picta marginata) Afflicted with Kyphosis
Abstract
Kyphosis, a congenital humpback condition of the spinal column, has been reported across a broad range of chelonian taxa. These reports are often of single observations and lack background information about the history of the animal(s) involved. A kyphotic female midland painted turtle (Chrysemys picta marginata) reported herein is a member of a long-term mark–recapture study in Algonquin Park (Ontario, Canada), providing a unique opportunity to document life-history characters of a kyphotic turtle over 18 yrs and draw comparisons to other members of her cohort and population. Despite her spinal deformity, the somatic growth, body size, age at sexual maturity, and reproduction of the kyphotic female have been similar to those of nonkyphotic females in our long-term study population, suggesting that the condition has not compromised her fitness.
Kyphosis is a rare, congenital humpback deformity of the spinal column (Ernst 1971; Rothschild et al. 2013). Numerous hypotheses have been proposed to explain the cause of kyphosis and other shell abnormalities in chelonians, but most explanations are related to developmental inconsistencies during embryonic or early juvenile development (Plymale et al. 1978; Wilhoft 1980; Rothschild et al. 2013). Kyphosis has been described across a broad range of chelonian taxa, including at least 7 families, 23 genera, and 27 species (Plymale et al. 1978; Rothschild et al. 2012, 2013).
Kyphosis has been described in painted turtles (Chrysemys picta; Cagle 1954; Rothschild et al. 2013). However, as with most reports of kyphotic chelonians, these isolated observations lack historical context for the individual(s) involved and rarely report potential effects on life history. Herein we report on somatic growth, maturity, and reproduction of a kyphotic female midland painted turtle (C. p. marginata) of known age from a long-term study.
Early History of Painted Turtle Id 7023a
A study on the life history of C. p. marginata has been ongoing since 1978 at Wolf Howl Pond (45°34′41.52″N, 78°41′21.39″W), Algonquin Provincial Park, Ontario. On 15–17 June 1996, eggs were collected from natural nests at the site, stored, and transported at 17°–20°C to the University of Guelph, where they were incubated at 29°C ± 0.2°C as part of a juvenile growth study (Koper and Brooks 2000). Painted turtle ID 7023A hatched on 30 August 1996 and was maintained in a laboratory over the winter of 1996–1997 (see Koper and Brooks 2000 for details on rearing conditions). The duration of the laboratory growth trial was 90 d, approximating the length of a single growing season in this northern population (Lefevre and Brooks 1995; Koper and Brooks 2000). The turtle was marked with notches in the marginal scutes (Cagle 1939) and released at Wolf Howl Pond in spring 1997. Thus, 7023A was head-started and experienced the equivalent of 2 growing seasons in the first year of its life.
Shell deformities were noted in 7023A at hatching and in subsequent years (N.K., pers. obs.). Shell defects included irregular bumps on the anterior marginal scutes; 6 vertebral scutes; a conical peaking of the third vertebral scute; a curved and upturned tail; and additional left plastral, left inframarginal, and right inframarginal scutes. The most readily identifiable deformity of 7023A is the hump-backed shape of the carapace (i.e., congenital kyphosis [Fig. 1]).
Citation: Chelonian Conservation and Biology 14, 2; 10.2744/CCB-1147.1
Growth, Body Size, and Age at Sexual Maturity
Following release in 1997, 7023A was first recaptured in Wolf Howl Pond in 2000 (and recaptured in 2004–2006) and later migrated to West Rose Lake (recaptured in 2008, 2010–2014), an overland distance of approximately 1 km. The turtle has a well-recorded growth history and a known age at sexual maturity (Table 1). We compared the growth of 7023A at release with the growth of free-living juveniles of known age from Wolf Howl Pond by plotting observed growth (Δ cm) against expected growth (Δ cm) of midline plastron length (PL) between successive observations (Fig. 2). Points on the 1:1 line indicate typical growth rates while points above and below the line indicate faster- and slower-than-expected growth, respectively (Fig. 2). Expected growth for each observation was calculated from PL at the beginning of the interval and elapsed time to the next observation using the von Bertalanffy interval equation (Fabens 1965) with parameters previously estimated from the study population (Samson 2003). Expected growth is positively related to interval duration and inversely related to PL. Plotted observations record growth intervals from 1 to 4 yrs (Table 1). All plotted intervals were treated as multiples of 1 yr because all observations of juveniles occurred in April or May, although nearly all growth occurs after 1 June in the study population (M.G.K., R.J.B., and J.D.L., unpubl. data, 2015). Growth intervals 7–10 for 7023A represent postmaturational growth (Table 1).
Citation: Chelonian Conservation and Biology 14, 2; 10.2744/CCB-1147.1
At the time of her initial release, 7023A was in the 84th percentile of midline PLs of known-age wild turtles starting their second growing season (n = 144) or in the 20th percentile of those starting their third season (n = 126) in the Wolf Howl Pond population. Therefore, in terms of PL, 7023A was intermediate in size between naturally hatched and overwintered turtles from the 1994 and 1995 cohorts.
Eleven years after release, 7023A was observed nesting in 2008 for the first time. Her chronological age at first observed nesting was therefore 12 yrs, but adjusted to approximately 13.5 yrs of age (size-wise) when accounting for her head start in the laboratory. At sexual maturity, 7023A had a PL of 12.98 cm and straight midline carapace length (CL) of 12.88 cm. At the time of her first nest, she was in the 34th percentile of PLs among a group of wild primiparous female painted turtles in the Wolf Howl Pond population (n = 47).
Nesting History
In her first observed reproductive season (2008), 7023A laid a clutch of 5 eggs. Despite intensive annual nest surveys at the above-mentioned sites, she was not recorded to be reproductively active from 2009 to 2011, but was found to have laid 2 clutches in 2012 (5 eggs and 7 eggs, respectively). In 2013 and 2014, 7023A was recorded demonstrating nest-site searching behavior, although no nests were observed.
Intrapopulational Comparison of Somatic Growth, Maturity, and Reproduction
The growth of 7023A has been comparable to that of natural recruits and head-started individuals of the same cohort (Fig. 2). In addition, size at sexual maturity of 7023A was consistent with that of typical females in the population. On average, female painted turtles in the Wolf Howl Pond population are primiparous at 13.0 cm PL (range, 12.1–14.2 cm), 13.1 cm CL (range, 12.12–14.19 cm), and 14.1 yrs of age (range, 12–15 yrs; Samson 2003). The chronological age at sexual maturity of 7023A is at the lower range recorded for females in the same population, although her adjusted age at sexual maturity (accounting for her head start) was comparable to that of typical free-ranging females (Samson 2003).
The primiparous clutch size of typical female painted turtles in the Wolf Howl Pond population ranges from 3 to 8 eggs (n = 45, 𝑥̄ ± SE = 5.96 ± 0.16). Thus, the primiparous clutch size for 7023A was also consistent with those of typical females in the population. Egg morphometrics (length, width, and mass) for 7023A were within the normal range of egg sizes for typical females in this population (R.J.B., unpubl. data, 2015). In painted turtle populations, 50%–70% (Moll 1973) and up to at least 82% (Iverson and Smith 1993) of females may reproduce annually. It is possible that 7023A nested but was not observed in some years despite intensive nesting surveys, because it is estimated that 10%–20% of nests are not directly observed in our study population each year (Rollinson and Brooks 2007). Because of the short nesting history of 7023A, we are unable to confirm whether her reproductive frequency, among other reproductive characters, is consistent with that of typical females in the Wolf Howl Pond population.
DISCUSSION
The reproductive capabilities and life-history characteristics of kyphotic turtles are seldom reported. Although she was afflicted with kyphosis, the growth, size and age at sexual maturity, and clutch size of Painted Turtle ID 7023A were comparable to those of other typical females in the population. This result is consistent with the findings that kyphosis seemingly does not influence male or female sexual maturity in the Australian species Emydura macquarii (Trembath 2009). Kyphosis did not impact overall body size, although it may have slowed growth in female ringed map turtles, Graptemys oculifera (Selman and Jones 2012). A kyphotic wood turtle, Glyptemys insculpta, was estimated to be smaller than expected for its age based on growth-ring counts (Harding and Bloomer 1979). In contrast, a more rapid mass gain, resulting in a better overall body condition, was recorded in a kyphotic juvenile snapping turtle (Chelydra serpentina) relative to nonkyphotic clutch mates raised in captivity (Wilhoft 1980).
The direct cause of kyphosis in 7023A is unknown, but occurred during the embryonic stage, given descriptions of the deformity at time of hatching (N.K., pers. obs.). From 2009 to 2013, 7023A was the only kyphotic turtle of the 947 individuals captured at our study sites. Thus, the frequency of kyphosis in the study population was only 0.11%. This very low prevalence of kyphosis is consistent with findings reported for sea turtles and freshwater turtles (reviewed by Rothschild et al. 2013). As with other reports in the literature (Ernst 1971, 1976; Plymale et al. 1978; Wilhoft 1980; Stuart and Painter 2008; Bujes 2009), the kyphotic condition reported here is accompanied by other abnormalities in scute number and arrangement.
We report the first long-term account of the life-history characters of a freshwater turtle with kyphosis and found that, despite the abnormality, the female turtle grew, reached maturity, and reproduced similarly to normal female turtles in the population. These findings suggest that kyphosis does not deleteriously impact individual fitness.
Painted turtle ID 7023A, adult female (in 2010). Note upturned tail and kyphosis, curvature of the spine. Photo by P. Moldowan.
Growth of kyphotic female painted turtle ID 7023A (n = 1, obs = 10, black circles with inset growth‐interval numbers; Table 1) compared with other individuals of contemporaneous cohorts. Observed growth (Δ cm) between successive observations of midline plastron length (PL) is plotted against expected growth (Δ cm). Growth observations of conspecifics that, like 7023A, were released in the spring of 1997 after being reared overwinter as part of a laboratory growth experiment (n = 10, obs = 101, gray circles; Koper and Brooks 2000) are symbolized separately from those of similar size that hatched in the wild between 1994 and 1996 and overwintered naturally (n = 8, obs = 51, gray triangles). Growth while 7023A was captive (prior to 1997; Table 1) was not included. Only females and juveniles (unknown sex or males with PL < 8.5 cm) are plotted. Expected growth for each observation was calculated from PL using the von Bertalanffy interval equation (see text). Symbols for growth intervals 7–10 are overlapping and represent postmaturational growth (Table 1).
Contributor Notes
Handling Editor: Peter V. Lindeman
