Hypomelanism in Irwin's Turtle, Elseya irwini, from the Johnstone River, North Queensland, Australia
Abstract
The occurrence of hypomelanism in a population of Irwin's turtles (Elseya irwini) was found to affect only adult turtles (approximately 10%), primarily females. Its complete absence in immature and hatchling turtles indicates that the condition develops ontogenetically through the progressive, localized loss of specific types of chromatophores. Hypomelanistic females were lacking in a variety of pigments affecting virtually all parts of the body and appeared to represent extreme forms of the natural depigmentation process that accompanies maturation in this species.
The occurrence of excessive or diminished amounts of melanin in the skin and scales of reptiles has been reported in a broad range of taxa (Dyrkacz 1981; Bechtel 1995; Majerus 1998) but comparatively few chelids (Lovich et al. 1990). Melanism (or hypermelanism) is the most commonly encountered example of this phenomenon and it has been the subject of study in the western painted turtle (Chrysemys picta bellii; Gronke et al. 2006), Reeves' turtle (Mauremys reevesii; Yabe 1994), the yellow-bellied slider (Trachemys scripta scripta; Lovich et al. 1990; Garstka et al. 1991), and the red-eared slider (Trachemys scripta elegans; McCoy 1966; Hays and McBee 2009). In these species melanism is only seen in males and develops at the onset of male (and sometimes female) sexual maturity, with size, and can be locality-specific (Lovich et al. 1990; Yabe 1994; Tucker et al. 1995; Stuart 1998). Melanism is known to develop with age in other chelids particularly, though not exclusively, in males (Lovich et al. 1990; Bonin et al. 2006). Hypomelanism by contrast has received comparatively little attention. It is a broad term that describes a set of conditions in which melanin is lacking and includes the readily identifiable conditions of axanthism, leucism, piebaldism, and albinism. Although examples of albinism among chelid species are not uncommon (e.g., Ewert 1979; Bechtel 1995), examples of other hypomelanistic conditions are. Most of these examples come from herpetoculturists, where they are reported to occur in both captive-bred and wild-caught turtle species, among them the Asiatic softshell turtle (Amyda cartilaginea), red-footed tortoise (Chelonoidis carbonaria), African spurred tortoise (Centrochelys sulcata), Mississippi map turtle (Graptemys pseudogeographica kohnii), false map turtle (Graptemys pseudogeographica pseudogeographica; Bartlett and Bartlett 2002), red-eared slider (Trachemys scripta elegans; Broghammer 2000), Barbour's map turtle (Graptemys barbouri), and painted turtle (Chrysemys picta; Ewert 1979). In T. s. elegans, the hypomelanistic “pastel” form that exhibits a predominance of yellow pigment is commonly available in the pet trade but is apparently uncommon in the wild (Lamer et al. 2007). Additionally there are two turtle species in which coloration naturally becomes lighter with age: Berlandier's tortoise (Gopherus berlandieri; Auffenberg and Weaver 1969) and the Fitzroy river turtle (Rheodytes leukops; Legler and Cann 1980); in the latter species the color change is confined to males and involves the apparent loss of melanin and its replacement with bright and contrasting colors on the head and neck. There do not appear to be any published reports concerning the frequency of hypomelanism in wild turtle populations. This suggests either a naturally low incidence of occurrence among chelids and/or a high mortality of affected individuals in the wild.
Irwin's turtle (Elseya irwini) occurs in the Burdekin and Johnstone river drainages of North Queensland, Australia. Until recently the Johnstone River populations were considered to be a separate taxon (Thomson and Georges 2010). Both sexes exhibit ontogenetic melanism of the shell, but the head and neck of females, in particular, undergo depigmentation and develop a “piebald” appearance (Cann 1998; Turner 2006). In Johnstone River populations the depigmentation process appears to occur through the localized loss of melanin and other pigments at or after maturity and typically involves the following changes in coloration: the head shield changes from dark gray/brown to predominantly or entirely mustard yellow; the nose changes from uniform dark gray/brown to partially or entirely pink; the face changes from dark gray to cream; the throat and underside of the neck change from pale gray/yellow to cream. In mature males the throat and face typically also develop cream patches though not to the same extent as in females. Cann (2008) stated that the carapace of female E. irwini from the Burdekin drainage often have large yellow patches covering 50% of the surface; however, this is not a feature of Johnstone River females (G.S. Turner, pers. obs.). Furthermore, Cann (2008) remarks that males from the Burdekin drainage develop a yellow head shield but only as “old adults” whereas the head shield of males from the Johnstone River remains dark gray/brown with no apparent color change (G.S. Turner, pers. obs.). Several other species from the Elseya dentata complex (of which E. irwini is a member) also exhibit ontogenetic changes in head and neck coloration, which are expressed most prominently, or exclusively, in mature females (Cann 1997, 1998; Thomson et al. 2006). Herein I document the frequency of occurrence of hypomelanism in a population of E. irwini from the Johnstone River, and describe a sample of 8 adult females that exhibit varying degrees of hypomelanism, affecting most or all parts of the body.
Methods
Hypomelanistic turtles were located incidentally as part of a broader study of E. irwini in the Johnstone River and its tributaries near Innisfail (lat 17°32′S, long 146°01′E), North Queensland, between 2003 and 2007 (see Turner 2006). Turtles were deemed to be sexually mature adults if they exhibited secondary sexual characteristics (i.e., longer and thicker tails in males, piebald coloration in females); turtles with a curved carapace length (CCL) < 50 mm were classed as hatchlings and all others as immature; sex could not be determined in turtles with CCL < 150 mm. A sample of the hypomelanistic turtles was briefly retained for examination. Turtles were scrubbed with a soft brush and then rinsed to remove silt, algae, and ectoparasites from the shell and skin, though it was not possible to remove all algae. Photographs of the dorsal, ventral, and head profiles of affected turtles were taken. Descriptions were made of turtles viewed under diffuse natural daylight. A hand lens (×10) was used to view the eye.
Results
Out of a total of 535 E. irwini examined, only 20 were found to exhibit hypomelanism (3.7%) and these were all adults, representing 9.6% of that size class (see Table 1). Significantly more females than males exhibited hypomelanism (17 vs. 3; 2 × 2 contingency table with Fisher's exact test, p = 0.008). Hypomelanism in males was comparatively rare and much more limited in its extent compared to females (see below).
No instances of hypomelanism were found in immature (n = 180) or hatchling (n = 147) turtles. Using the adult data to generate the expected frequencies for both these classes, the probability of obtaining these results due to chance was very small (p < 0.00001 in both instances; binomial distribution, p = 0.096), with the expected number of affected immature and hatchling turtles being 14 and 17 respectively. These results indicate that the hypomelanism observed in adults is ontogenetic.
Figure 1 shows 8 females approximately ordered from greater to lesser extremes of hypomelanism. Females were similar in size (CCL range, 47 mm) and sexually mature (CCL > 205 mm; Turner 2006). In Table 2, the coloration of the hypomelanistic females is described with respect to 8 locations on the head, neck, limbs, and shell, and is compared to a typically pigmented female. Several minor differences exhibited by the hypomelanistic females were omitted from the table. For example, the tail color of all hypomelanistic females was dark gray above, but unlike typically colored females, it was mostly cream below and often the skin around the cloacal opening was pink (e.g., females 2, 3, and 5). A further 9 hypomelanistic females were located during the study and their appearance was within the range exhibited by those described in Table 2. In males hypomelanism was limited to the presence of small white patches on the upper surface of the tail; one male also showed significant areas of white spotting and blended white and gray patches on both the upper and lower surfaces of the back limbs.
Citation: Chelonian Conservation and Biology 10, 2; 10.2744/CCB-0851.1
Females 1–3 (Fig. 1a–c) were particularly striking in their appearance, as the carapace was predominantly yellow, revealing the costal sutures; the plastral sutures were also clearly visible. White areas of skin, indicating a complete lack of pigment, were evident on 2 or more limbs of these females and was strongly contrasted with the normal dark gray coloration (Fig. 2a). The undersides of the limbs, tail, and axillary pockets of most affected females were white with a diffuse blue-gray pigment forming blotches and irregular patterns (Fig. 2b). In most females, dark gray coloration was confined to the top of the neck where it was strongly demarcated from the white/cream skin that bordered it. White patches on the sclera that occurred in most of the females did not extend onto the iris. Claw coloration was affected to different degrees with a tendency for the innermost claws to be paler than the others. Female 8 most closely resembled a typical mature female in coloration, with the carapace almost entirely black and only a few white (unpigmented) spots on the limbs.
Citation: Chelonian Conservation and Biology 10, 2; 10.2744/CCB-0851.1
Females 1 and 4 were recaptured 3 and 1.5 years later, respectively, and neither showed any increase in size; a comparison with photographs taken when they were first examined failed to detect any change in the distribution of pigments.
Discussion
Hypomelanistic female E. irwini exhibited varying degrees of depigmentation affecting nearly all parts of the body: the skin, shell, head shield, eyes, and claws. The gray iris and blended blue-gray skin of the axillary pockets of affected females is consistent with the absence of properly functioning melanophores and xanthophores. Depigmentation of the carapace resulting in yellow regions suggests a loss of melanophores but not xanthophores. Pure white patches of skin are indicative of a complete lack of functioning chromatophores. It is evident from these examples that the depigmentation process is not spatially uniform and therefore that the combination of functioning chromatophores varies locally. It is also evident that the term hypomelanism is not an entirely satisfactory descriptor of the condition exhibited by female E. irwini, as clearly melanin is not the only pigment that is involved in the depigmentation process. The appearance of affected females resembles vitiligo, a condition that typically involves the ontogenetic (partial or complete) loss of melanin from the epidermis, resulting in the development of white patches of skin surrounded by normal skin (Bechtel 1995). The condition is known to occur in reptiles, though is poorly understood and is reported less often than conditions such as albinism.
Changes to melanin (and other pigments) in the skin and shell of freshwater turtles can be described as permanent (unchanged throughout life), reversible (i.e., can change depending upon season, breeding condition, substrate color), and ontogenetic (changes with age) (see Lovich et al. 1990). Hypomelanistic conditions such as albinism, xanthism, leucism, and piebaldism are known to be congenital and therefore permanent (see Dyrkacz 1981; Bechtel 1995). In E. irwini there were no examples of hypomelanistic immature or hatchling turtles, despite relatively large sample sizes, indicating that the hypomelanism exhibited by adults is ontogenetic and that a gradual localized loss of melanin (and other pigments) occurs at or after sexual maturity. Females of the species naturally undergo localized depigmentation, though to a much more limited extent than the sample females described above. Thus the sample females appear to represent extreme forms of this natural depigmentation process.
The incidence of hypomelanism in the adult population of E. irwini was relatively high (approximately 10%) and turtles examined from other sections of the river and its tributaries have not exhibited the condition, although sample sizes are considerably smaller (ca. 60 adults; G.S. Turner, unpubl. data). Hypomelanism was not recorded in 2 other studies of the species that sampled populations in other tributaries and the upper reaches of the North Johnstone River (O'Malley 2007; Freeman and Curran 2009). This suggests that hypomelanism may be confined to the source population and may have arisen through a localized genetic variant.
There are several reasons why hypomelanism in E. irwini may not be strongly selected against: 1) immature and hatchling turtles do not exhibit hypomelanism and they frequently inhabit clear shallow water and rely on crypsis to avoid detection, 2) turtles of all sizes have an algal and silt coating on the shell and skin which tends to conceal paler colors, 3) the benthic habit of this species may afford some protection from terrestrial predators that rely primarily on vision to detect prey, and 4) adult turtles appear to have few predators (G.S. Turner, pers. obs.).
Photos of the 8 sample hypomelanistic female Johnstone River Elseya irwini: (a) Female 1, (b) Female 2, (c) Female 3, (d) Female 4, (e) Female 5, (f) Female 6, (g) Female 7, and (h) Female 8. (Photos by G.S. Turner.)
(a) The back foot of Female 2 showing extensive areas of white unpigmented skin. (b) Ventral view of Female 5 showing a blended mosaic of white and blue-gray skin on the underside of the limbs. (Photos by G.S. Turner.)
