First case of conjoined twins in the Quince Monitor Lizard Varanus melinus Böhme & Ziegler, 1997

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1 Herpetology Notes, volume 7: (2014) (published online on 21 December 2014) First case of conjoined twins in the Quince Monitor Lizard Varanus melinus Böhme & Ziegler, 1997 Mona van Schingen 1, 2, * and Thomas Ziegler 1, 2 Abstract. We report on the first case of conjoined twinning in the Quince Monitor Lizard Varanus melinus and provide a detailed morphological description of abnormally developed offspring. Parents were siblings and produced two clutches which both contained normally developed, viable offspring next to unfertilized eggs and malformed, dead individuals. This also is the first report on the development of conjoined twins in the Pacific monitor lizard species group, and the second case of conjoined twinning reported for monitor lizards in general. We further present an overview of published cases of twinning and the development of malformations in reptiles as well as potential causes such as genetic or environmental factors. Keywords: Squamata, Varanidae, monozygotic twinning, malformations, morphology. Introduction Several cases of twinning have been reported for diverse taxa of reptiles, such as turtles (Lehmann, 1984; Piovano et al., 2011), crocodiles (Platt et al., 2001), snakes (Kinkaid, 1996) and lizards (Mendyk, 2007). With respect to monitor lizards, cases of twinning have been reported for eight species: Varanus gouldii (Hartdegen and Bayless, 1999), V. indicus (Speer and Bayless, 2000), V. kordensis (Jacobs, 2002), V. macraei (Mendyk, 2007), V. mertensi (Eidenmüller and Stein, 1991), V. ornatus (Mendyk, 2007), V. panoptes horni (Bayless, 1999) and V. semiremex (Jackson, 2005). In addition, a case of triplets has been reported for V. varius by Krauss and Horn (2004). However, cases of conjoined twins in reptiles are much rarer. Several reports of this phenomenon exist for turtles (Mähn, 1997; Sailer et al., 1997; Stumpel, 2008), crocodiles (Youngprapakorn et al., 1994; Webb and Manolis, 1998; Velasco, 2010) and 1 Cologne Zoo, Riehler Straße 173, 50735, Cologne, Germany 2 University of Cologne, Institut of Zoology, Department of Terrestrial Ecology, Zülpicher Straße 47b, 50674, Cologne, Germany * Corresponding author mschinge@smail.uni-koeln.de lizards, such as agamids (Förther, 2002) and gekkonids (Rösler, 1979). Concerning monitor lizards, reports of conjoined twins are only known for members of the emerald tree monitor lizard (Varanus prasinus) species group. Jacobs (2002) reported a case of an individual with a twofold developed head due to cross breeding between the closely related species V. kordensis and V. prasinus. Recently, Ziegler et al. (2010) reported on the first F2 reproduction of the Quince monitor lizard, V. melinus Böhme and Ziegler, 1997, a Moluccan species of the V. (Euprepiosaurus) indicus group. Parents held at the Cologne Zoo Terrarium were siblings and produced two clutches deposited in June and September 2009 consisting of nine and five eggs, of which six and two individuals finally hatched. Of the first clutch, two eggs did not show any development and one egg contained dead conjoined twins. The eggs of the second clutch contained two eggs without development and another egg containing a dead, malformed offspring. We herein provide a morphological description of the abnormalities of both the conjoined twins and the malformed sibling, compared with normally developed V. melinus, considering anatomy, morphometry, osteology and pholidosis. Besides documenting the first case of conjoined twins in a member of the Pacific monitor lizard (V. indicus) species group we further discuss potential causes for the development of such malformations.

2 724 Materials and methods The conjoined twins and the malformed hatchling of Varanus melinus were preserved in 70 % ethanol and deposited in the herpetological collection of the Zoologisches Forschungsmuseum Alexander Koenig (ZFMK) in Bonn, Germany. ZFMK 96604a and ZFMK 96604b refer to the twins and ZFMK to the malformed individual. Morphological and meristic data (see Böhme and Ziegler 1997) were taken by dint of a stereo microscope (Leica MS5). For the measurements (to the nearest 0.1 mm) a caliper was used. To determine the kind of divergence of the abnormal individuals, the accordant data from the type series as given in Böhme and Ziegler (1997) was used as a reference. In addition, a normally developed, but deceased juvenile of V. melinus (ZFMK 96606) with an age of maximally 10 months, which derived from the clutches deposited between June and September 2009 and thus descending from the same parents was used for direct comparisons. For the study of the bone structure a radiogram was made with a Faxitron X-Ray Lx60. Mona van Schingen & Thomas Ziegler Abbreviations are as follows: SVL: snout-vent length, from tip of snout to cloaca; TaL: tail length from cloaca to tip of tail; ToL: total length, tip of snout to tip of tail; A: head length, from tip of snout to tip of tail; B: head width, maximum width between eyes and ears; C: head height, above the eyes; G: distance from anterior eye margin to middle of nostril; H: distance from middle of nostril to tip of snout; ElHa: length from elbow to insertion of hand; Thorn: length of a thorn-shaped scale formation at the neck on the right body side; P: scales across head from rictus to rictus; Q: scales around tail base; R: scales around tail at approximately one-third from base; S: scales around midbody; T: transverse ventral scale rows from gular fold to insertion of the hind legs; N: gular scales from tip of snout to gular fold; AG: scales from axilla to groin; TN: ventral scales from tip of snout to insertion of hind legs; X: transverse dorsal scale rows from hind margin of tympanum to insertion of hind legs; c: supralabials exclusive the rostral scale; Sub: sublabials exclusive the mental scale; M: scales around neck anterior to gular fold; U: differentiated (= enlarged) supraocular scales. Figure 1. Conjoined twins (ZFMK 96604a, b) of Varanus melinus. A: Twins in egg; B: Cranial adhesion of the twins; C: Abdominal adhesion; D: Egg tooth of ZFMK 96604a. Photos: T. Ziegler.

3 First case of conjoined twins in the Quince Monitor Lizard 725 Table 1. Mensural and selected meristic data of the conjoined twins (ZFMK96604), the malformed sibling (ZFMK 96605), and a normally developed specimen (ZFMK 96606) of Varanus melinus compared to the type series (after Böhme and Ziegler 1997). For abbreviations see material and methods; all measurements in mm. Bilateral values are given as left / right. Abbreviation ZFMK96604a ZFMK96604b ZFMK ZFMK Type series SVL TaL ToL A 19.8 / / / B C G 5.0 / / / H 5.1 / / / ElHa 14.2 / / / Thorn G/H 0.98 / / / A/B 1.82 / / / A/C 2.54 / / / P Q R S T / N / AG 67 / / / / TN (=T+N) / X 36 / / / c 27 / / / Sub 27 / / / / 26 - M U 5 / 4 3 / 4 0 / / 5 - Results Morphometric data and scale counts of the conjoined twins (ZFMK 96604a and ZFMK 96604b) and the malformed hatchling (ZFMK 96605) in comparison with the normally developed juvenile (ZFMK 96606) and respective data of the type series (Böhme and Ziegler, 1997) are shown in Table 1. Description of the conjoined twins (ZFMK 96604a and ZFMK 96604b) The twins are both cranially and abdominally (over abdominal-tissue) conjoined (so called cephalothoracopagus conjoined twins), generally well developed and have entire extremities and tails. However, the belly of both individuals is open (Fig. 1, A-C). Both individuals have distorted vertebral columns, which is visible from the radiogram (Fig. 2). The smaller specimen (ZFMK 96604b), has less developed extremities than ZFMK 96604a and a truncated body (Fig. 1C). The vertebral column of ZFMK 96604a is curved to the dorsum (Fig. 2), and that of ZFMK 96604b is likewise bound upwards and additionally looped at the midbody, while the trunk is folded (Fig. 2). The head of ZFMK 96604a is laterally bent, with the mental scale being displaced from frontal to lateral. The upper jaw is reduced and the snout notched in position of the egg tooth while the lower jaw overhangs (Fig. 1, D). Concerning the mouth part, ZFMK 96604b also shows malformations, namely a reduction of the left mouth part, discernible in the distinctly lower number of labial scales (13 vs. 21 sublabials and 16 vs. 22 supralabials, see Table 1). Furthermore the left hind leg of ZFMK 96604b terminates in two separated feet, which are aligned between first and second toes (Fig. 2). One foot

4 726 Figure 2. Radiogram of the conjoined twins (ZFMK 96604a, b) of Varanus melinus. contains six toes, of which two are truncated and end in a thickened claw. The foot of the right hind limb features two coadunate toes. Both twins dorsolaterally show a Mona van Schingen & Thomas Ziegler thorn-shaped formation of scales on their right body side behind the gular fold. With respect to scalation the specimen ZFMK 96604b further differs from its sibling, the normally developed specimen and the type series (see Table 1) in having less scales around the tail base (64 versus 81 85), and less ventral scale rows between the gular fold and the insertion of the hind limbs (56 versus 87 99). ZFMK 96604a has a reduced number of scales around the midbody compared with the normally developed specimen and the type series (98 versus ). Both conjoined twins have a distinctly lower number of gular scales (49 56 versus 84 89) and a reduced number of ventral scales between the snout and the hind limbs ( versus ), compared with the normally developed specimen and the type series. Furthermore we found differences between the two body sides in both siblings: ZFMK 96604b has 56 and 29 ventrolateral scales between the insertions of the fore- and hind limbs on its two body sides, while ZFMK 96604a has about ventral scales on each side, which is distinctly fewer than the 105 scales counted in the normally developed individual (ZFMK 96606); ZFMK 96604a in addition shows an asymmetry in fore Figure 3. Malformed Varanus melinus (ZFMK 96605). A: Curved vertebral column; B: Opened vent; C: Malformed cranium; D: Lateral thorn-shaped formation of scales. Photos: T. Ziegler.

5 First case of conjoined twins in the Quince Monitor Lizard 727 and Böhme (1999) for an adult male V. melinus. The sulcus spermaticus is discernible, stretching terminally to the outer lobe. The apical platform is asymmetrically prolonged towards the outer lobe. Terminally, from both asymmetrical lobes, the two elastic hemibacula are protruding. The inner hemibacula are larger, shovelshaped, apically-directed and with broadened ends. The smaller, outer and laterally-oriented hemibacula are also discernible. At the outer lobes there are hints of paryphasman rows discernible. Discussion Figure 4. Radiogram of the malformed individual (ZFMK 96605) of Varanus melinus. limb lengths (elbow-hand on the left 14.2 mm vs mm on the right, see Table 1). Description of the malformed hatchling (ZFMK 96605) The vertebral column of ZFMK (see Fig. 3) is flexed at the most posterior part of the trunk and the insertions of the hind limbs are not symmetrically developed, which is apparent from the radiogram (Fig. 4). The following asymmetries in the outer body shape were noted: abnormal proportions of the head; truncated maxilla; overlaying and right-bent mandible; rostral scale being in contact with the third left sublabial scale instead of the mental scale; cut from the left nostril to the middle of the third and fourth supralabial and a cranial swelling on the front between the eyes (Fig. 3). With respect to the normally developed specimen and the type series, the individual ZFMK furthermore differs in the following characters: notched tail base and thus less scales around tail base (69 vs ); a greater number of scales around the midbody (144 vs ) and a lower number of ventral scales on the right body side (170 left, 142 right vs ventral scale rows from snout to insertion of hind limbs). Furthermore, ZFMK dorsolaterally shows a thorn-shaped formation of scales on the right side, pointing to the dorsolateral fold. Both hemipenes of ZFMK are everted (Fig. 5). They are longish, passing apically into two asymmetrically-shaped lobes as described by Ziegler The three analyzed, malformed hatchlings of Varanus melinus differ in several traits from normally developed individuals. The conjoined twins are noticeably smaller compared to their normally developed siblings (SVL 49.6 and mm versus mm, see Ziegler et al., 2010). Also the malformed individual ZFMK is slightly smaller (SVL 91.1 mm). However, the fact that terminal structures (such as spikes and spines) are not discernible in the hemibacula of the individual ZFMK cannot be regarded as malformation, because such indifferent development might be due to the developmental stage. This is also the reason for the everted condition of the hemipenes, which in general are only retracted into the tail base shortly before hatchling (e.g., Ziegler and Böhme, 1997). The three analyzed, malformed individuals differ with respect to modified scale counts, malformations of body parts and thus also proportions from normally developed individuals. Figure 5. Everted hemipenes of the malformed Varanus melinus (ZFMK 96605). Photo: T. Ziegler.

6 728 The conjoined twins also differ from each other and show asymmetries in scalation even between their own body sides. But the differing scalation apparently does not follow a general principle, as e.g., one of the conjoined twins (ZFMK 96604a), and the malformed individual ZFMK developed increased numbers of scales around the gular fold (100 and 104) whereas the other twin (ZFMK 96604b) rather showed a reduced number of scales around the gular fold (68) compared to normally developed individuals (83 90). But in general a tendency towards scale number reduction is discernible, most apparently in the individual ZFMK 96604b. This individual is also the less developed and smaller conjoined twin. The case that one conjoined twin is better developed than the other one was also reported by Rösler (1979) and Eidenmüller and Stein (1991). In addition, the ratios of measurements (G/H, A/B, A/C, see Tab. 1) show that the proportions of the abnormal hatchlings of V. melinus differ remarkably from the type series. All three analyzed malformed hatchlings have a relative broader, shorter and higher head and show a different position of the nostril between the snout and eye. Although the three malformed individuals show distinct differences compared with the type series, from each other and their own body sides, we found some joint features, such as an opened vent, a curved or flexed vertebral column and a lateral thorn-shaped skin structure. Here, it is interesting to note that the three malformed individuals all derived from the same parents but developed from different clutches. Thus, genetic predispositions as reason for the development of identical or at least similar malformations cannot be excluded, in particular as the parents were related to each other. A low genetic variation is frequently contemplated as reason for the development of malformations (e.g., Gautschi et al. 2002). In addition, conjoined twinning and the generating of further malformations apparently is often linked (e.g., Mähn, 1997; Rösler, 1997; Förther, 2002; Jacobs, 2002). Concerning the occurrence of conjoined twins, Sailor et al. (1997) reported one case of well-developed conjoined twins (only with anomalies in the lateral shields) in the turtle Testudo hermanni boettgeri over a period of ten years (opposed to 98 healthy offspring hatched from 117 eggs, which all were treated under the same conditions). Another isolated case of conjoined twins (which were cranially conjoined, but otherwise fully developed and which died shortly before hatching) was reported for the agamid Pogona vitticeps, which was successfully bred for a noticeable period of time (Förther, 2002). With respect to conjoined twins in monitor lizards, Jacobs (2002) described a case of conjoined twins as an outcome of the cross breeding between the closely related species V. kordensis and V. prasinus. Two of three fertilized eggs included embryos, which died before hatching. The remaining egg contained a specimen with a twofold developed head, three forelegs but only one abdomen and tail. This individual proved not to be viable and died quickly after hatching. Similar to the situation in V. melinus reported herein, the hybrid between V. kordensis and V. prasinus showed a strongly curved backbone and an opened vent with some organs being arranged outside of the body. Mähn (1997) supposed, that the disposition of the parents might be a cause for the development of twins (see also Heimann 1993). Further evidence for a correlation between the development of malformations and the genotypic variability of the parents was given by Gautschi et al. (2002). These authors found out that the snake Natrix tessellata showed an increased development of anomalies in introduced, bottlenecked populations, implicating a lower genetic variability than in native populations. Another cause for the development of malformations was given by Velsaco (2010), who found an individual of the crocodile species Crocodylus acutus with a twofold body and 8 extremities in a clutch in the National Park Laguna de Tacarigua, Venezuela, which is under influence of chemicals from agriculture. In general, malformations can derive based on genetic or environmental influences (Youngprapakorn et al., 1994). Such phenomena can be traced back to the lower Cretaceous for choristoderan reptiles (Buffetaut et al., 2007). However, a potential relation between relatedness of parents and probability of occurrence of malformations and conjoined twins, which could be possible based on the herein reported case, still needs further verification and research. Acknowledgements. We thank the ichthyology section of the ZFMK (Dr. Fabian Herder) for kindly taking radiograms. References Mona van Schingen & Thomas Ziegler Bayless, M.K. (1999): Varanus gouldii horni: twins. Dragon News 2: 4. Böhme, W., Ziegler, T. (1997): Varanus melinus sp.n., ein neuer Waran der V. indicus- Gruppe von den Molukken, Indonesien. Herpetofauna 19: Buffetaut, E., Jianjun, L., Haiyau, H., Zhang, H. (2007): A twoheaded reptile from the Creataceous of China. Biology Letters, 3: Eidenmüller, B., Stein, R. (1991): Zwillingsanlage bei Varanus mertensi (GLAUERT, 1951). Salamandra 27:

7 First case of conjoined twins in the Quince Monitor Lizard 729 Förther, R. (2002): Siamesische Zwillinge bei Bartagamen Pogona vitticeps. Herpetofauna 24: 34. Gautschi, B., Joshi, J., Widmer, A., Koella, J.C. (2002): Increased frequency of scale anomalies and loss of genetic variation in serially bottlenecked populations of the dice snake, Natrix tessellata. Conservation Genetics 3: Hartdegen, R.W., Bayless, M.K. (1999): Twinning in lizards. Herpetological Review 30: 141. Heimann, E. (1993): Drei Zwillingspaare bei Testudio marginata. Salamandra, 29: Jackson, R. (2005): The poorly known Rusty Monitor Varanus semiremix: history, natural history, captive breeding and husbandry. Herpetofauna 35: Jacobs, H.J. (2002): Zur morphologischen Variabilität der nominellen Smaragdwaran-Taxa Varanus prasinus (H. Schlegel, 1839) und V. kordensis (A.B. Meyer, 1874), mit Bemerkungen zur Erstzucht des Letzteren. Herpetofauna 24: Krauss, P., Horn, H.G. (2004): Triplet Lace Monitors (Varanus varius) hatching from one egg. Reptiles Australia 1: Kinkaid, J.F. (1996): Pseudechis coletti (Collet s Blacksnake). Twinning. Herpetological Review 27: 26. Lehmann, H. (1984): Ein Zwillingsschlupf bei Sternotherus minor minor (AGASSIZ, 1857). Salamandra 20: Mähn, M. (1997): Siamese twins of Testudo marginata (Schoepff, 1792). Salamandra 32: Mendyk, R. (2007): Dizygotic Twinning in the Blue Tree Monitor, Varanus macraei. Biawak 1: Piovano, S., Kaska, Y., Prazzi, E., Nannarelli, S., Giacoma, C. (2011): Low incidence of twinning in the loggerheas sea turtle. Folia Zoologica 60: Platt, S.G., Raiwater, T.R., McMurry, S.T. (2001): Twinning in Morelet s Crocodile (Crocodylus moreletii) and brief review of twinning in crocodilians. Herpetological Natural History 7: Rösler, H. (1979): Eine siamesische Zwillingsbildung bei der Gecko-Species Crossobamon eversmanni. Salamandra 15: Sailer, A., Pyczak, C., Hartmann, U. (1997): Siamesische Zwillinge bei Testudo hermanni boettgeri. Herpetofauna 19: Speer, R.J., Bayless, M.K. (2000); The first report of mangrove monitor twins in captivity: the remarkable reproduction and disappointing result. Reptiles 8: Stumpel, J. (2008): Conjoined twins in an egg from a three-striped mud turtle (Kinosternon baurii, Garman, 1891). Schildkröten im Fokus 5: Velasco, A. (2010): Rare abnormal Crocodylus acutus hatchling. Crocodile Specialist Group Newsletter 29: Webb, G., Manolis, C. (1998). Australian Crocodiles. A Natural History. Reed New Holland Australia. Youngprapakorn, P., Ousavaplangchai, L., Kanchanapangka, S. (1994): A color atlas of diseases of the crocodile. Bankok, Chulalongkorn University. Ziegler, T., Böhme, W. (1997): Genitalstrukturen und Paarungsbiologie bei squamaten Reptilien, speziell den Platynota, mit Bemerkungen zur Systematik. - Mertensiella, Rheinbach 8: Ziegler, T., Böhme, W. (1999): Genital morphology and systematics of two recently described monitor lizards of the Varanus (Euprepiosaurus) indicus group. Advances in monitor research II. Mertensiella 11: Ziegler, T., Rütz, N., Oberreuter, J., Holst, S. (2010): First F2 Breeding of the Quince Monitor Lizard Varanus melinus Böhme & Ziegler, 1997 at the Cologne Zoo Aquarium. Biawak 4: Accepted by Christoph Liedtke