Volume 306, Issue 3 p. 688-691
COMMENTARY
Free Access

A rare case of caudal bifurcation in a miniaturized gecko from Puerto Rico

Juan D. Daza

Corresponding Author

Juan D. Daza

Department of Biological Sciences, Sam Houston State University, Huntsville, Texas, USA

Correspondence

Juan D. Daza, Department of Biological Sciences, Sam Houston State University, Huntsville, TX, USA.

Email: [email protected]

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Ylenia Chiari

Ylenia Chiari

Department of Biology, George Mason University, Manassas, Virginia, USA

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Emilia Daza-Herrera

Emilia Daza-Herrera

Scott Johnson Elementary and Huntsville Intermediate School, Huntsville, Texas, USA

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Mayim S. Glaberman

Mayim S. Glaberman

Laurel Ridge Elementary School, Fairfax, Virginia, USA

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Scott Glaberman

Scott Glaberman

Department of Environmental Science and Policy, George Mason University, Fairfax, Virginia, USA

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Olivia A. Heide

Olivia A. Heide

Department of Biological Sciences, Sam Houston State University, Huntsville, Texas, USA

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Alexandra Herrera-Martínez

Alexandra Herrera-Martínez

Diagnostic Laboratory for Human Health, Sam Houston State University, Huntsville, Texas, USA

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Richard Thomas

Richard Thomas

Biology Department, University of Puerto Rico, Río Piedras Campus, Río Piedras, Puerto Rico

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First published: 06 July 2022

Funding information: Department of Biological Sciences Sam Houston State

Geckos from the genus Sphaerodactylus are part of a New World radiation of the family Sphaerodactylidae, including the genera (Chatogekko, Coleodactylus, Gonatodes, Lepidoblepharis, and Pseudogonatodes). This New World clade is often referred to as sphaerodactyls (Grant, 1932; Kluge, 1995). Spherodactyls are secretive and elusive (Barbour, 1921; Schwartz, 1973), and because they are unusually small, they are most of the time unknow by locals. Some of them can measure only 25 mm (including the tail), making them one of the smallest living amniotes (Hedges & Thomas, 2001; Thomas, 1965). Spherodactyls also occupy a comparable position in the food web as small arthropods due to their diminutive size (Vitt et al., 2005).

While sampling populations from high elevation localities in the cordillera Central and the Yunque massif, as part of an ongoing long-term survey of miniaturized geckos from Puerto Rico (Daza et al., 2019), we discovered an unusual specimen of Sphaerodactylus cf. klauberi with a terminal caudal bifurcation.

1 SPECIMEN

The specimen was found at an altitude of 303 meters in Las Marias town, Barrio Palma Escrita (informally known as “El pueblo de la china dulce”; china refers to the orange citrus fruit in Puerto Rico). The specimen was identified as Sphaerodactylus cf. klauberi. Its distribution is equivalent to Sample I (sensu Thomas & Schwartz, 1966), and phenotypically resembles an undescribed species of Karst-endemic Sphaerodactylus, previously allied with S. klauberi (Díaz-Lameiro et al., 2013) and currently under description (Diaz-Lameiro et al., 2022). Some similarities with the Karst-endemic species include the small size, dark coloration, and the presence of a triangular dark parietal figure (although in the Karst geckos, this figure tends to be more pentagonal; JDD personal observation).

The specimen was collected on May 22, 2022 around 17:11 p.m. next to an abandoned house (Permiso de colecta DRNA: 2021-IC-065, specimen housed at Texas Memorial Museum, Texas Natural History Collection, TNHC 116659). A total of three specimens were found, two of Sphaerodactylus cf. klauberi (one juvenile and a subadult) and one adult of Sphaerodactylus grandisquamis spanius. The specimen with bifurcated tail is a subadult, and although the parietal fontanelle is closed, the epiphyseal plates of long bones and carpus, tarsus elements are still cartilaginous, indicating that tail regeneration occurred at an early ontogenetic stage (Figure 1).

Details are in the caption following the image
Live specimen of Sphaerodactylus cf. klauberi with regenerated and bifurcated tail (above). X-rays of the specimen (TNHC 116659) showing the skeletal anatomy, especially the terminal portion of the bifurcated tail (below)

2 SPECIMEN PREPARATION AND IMAGING

The specimen was euthanized and preserved following protocols in Gamble (2014). It was fixed using 10% buffered formaldehyde, and then transferred to 70% ethanol. Before euthanasia, live pictures of the specimen were taken using a digital camera Leica V-LUX (Figure 1). Digital X-rays of the fixed specimen were obtained using a Thermo Scientific™ PXS5-927 microfocus X-ray source and a Mars 1717 V Wireless a-Si Flat Panel Detector (Figure 1).

3 ANATOMICAL OBSERVATIONS

Bifurcated tails have been reported in other geckos (Barr et al., 2020), and recently the first case within the family Sphaerodactylidae has been reported (using four specimens of the gecko endemic to Morocco Quedenfeldtia trachyblepharus, Mouadi et al., 2021). To the best of our knowledge, however, this is the first case reported among geckos within the New World radiation, despite the long-term work in this group of geckos by some of us (RT and JDD) and more than 60 years of collecting these geckos in the Caribbean (see also Bauer et al., 2021). In comparison with the geckos illustrated by Mouadi et al. (2021), the patterns of tail regeneration (i.e., bifurcation with a short abnormal growth, narrow bifurcation, extra growth presumably after an incomplete tail break, and trifurcated tail) are different than the one observed here.

The bifurcated tail in the specimen TNHC 116659 follows the pattern described as a large regeneration bifurcation event (Barr et al., 2020), with one side slightly shorter and thinner. The left side (dorsal area 4.1 mm2) is 1.6 times larger than the right tail (dorsal area 2.5 mm2; areas calculated using ImageJ, Schneider et al., 2012). The bifurcation was produced by tail autotomy at the level of the 17th vertebra. The left side developed a cartilaginous axial rod that is 151° from the vertebral column (41° between both tails). The 16th vertebra shows some bending toward the left at the autotomy plane, and only half of the 17th vertebra is preserved. The scales are similar to the rest of the tail, being acute, imbricated and keeled. The right side is slightly shorter and has a cartilaginous rod that extends from the autotomy plane of the 16th vertebra, but apparently not extending to the end of the right tail.

4 IMPLICATIONS OF BIFURCATED TAIL REGENERATION

It has been observed that when a lizard autotomizes its tail, but this process is incomplete or there is a sufficient caudal wound, an additional tail can be formed (Barr et al., 2020; Dudek & Ekner-Grzyb, 2014). This is frequently documented in the literature, including early illustrations from the 18th and 19th centuries (see Barr et al., 2020). We know based on an extensive recent review that abnormal regenerated tails were found in 22 families of limbed lepidosaurs (Barr et al., 2020), which includes Sphenodon and lizards.

Based on initial observation of the tail, we assumed it was an original tail due to the similarity of the scales to the rest of this appendage. The external morphology of the regenerated tail in lizards can be different from the original tail, especially if the regeneration process includes a prolonged inflammatory period, which might be associated with scarring (Alibardi, 2010; Eming et al., 2017). However, previous studies of lizards (including geckos) have found that the morphology of scales may differ when the skin is recreated, even without scarring (Peacock et al., 2015; Woodland, 1920; Wu et al., 2014). In the case of Sphaerodactylus geckos, the scales of regenerated tails frequently look different than the rest of the tail (JDD, AH-M Personal observation). However, in Teratoscincus and other sphaerodactyl geckos, the caudal scales are usually regenerated together with the new tail (Werner, 1967). In addition to tail autotomy, Sphaerodactylus geckos are also notorious for having skin with a low tensile strength, which is readily shed and regenerated, and has been described as an important additional predator escape mechanism from some arthropods (Bauer et al., 1992).

In geckos, tail regeneration has been described in several stages: a sequence of different structural changes including an initial retraction of the spinal cord, proliferation of cells at the wound site, regeneration of a simple spinal cord (ependymal cells and nerve tracts), and formation of cartilaginous support surrounding the spinal cord (Gilbert & Vickaryous, 2018). It has also been proposed that, in lizards, the replacement of individual vertebra by a single cartilaginous rod coupled with the loss of regularly spaced interdigitated muscles might produce a reduction of fine movements in the regenerated tail (Ritzman et al., 2012). A more rigid two thirds of the tail in Sphaerodactylus could potentially affect their social display, as tail waving is a common behavior among these geckos (Leuck et al., 1990).

The X-ray of the tail of the specimen TNHC 116659 clearly indicates that the regeneration of the bifurcated tail is product of a single event, where the left tail was regenerated from the complete break at the autotomy plane of vertebra 17th, and the right tail originated from a wound in the autotomy plane of vertebra 16. The smaller diameter of the right tail compared to the left tail might be representing a simpler supporting cartilaginous rod, which might constrain the amount of muscle tissue.

Although reports on tail bifurcation are common in the literature, these reports frequently are limited to photographs or drawings, without data from the axial skeleton. In fact, even when internal anatomy data is presented (e.g., microCT data the skink Egernia kingii, Barr et al., 2020), no details are provided about the exact vertebral position where this occurred. More precise information about the position of the autotomy plane and the regeneration would better describe this regeneration anomaly. Future studies can also provide experimental data involving injuries on different vertebrae, for example, surgical deviation of the spinal cord in eublepharid geckos generated an ectopic tail (Whimster, 1978). Detailed data of regenerated tails and experimentation can help better understand the multiple patterns of regeneration of multiple tails in lepidosaurian reptiles.

FUNDING INFORMATION

Grant sponsor: Department of Biological Sciences Sam Houston State.