First case of conjoined twins in the Quince Monitor Lizard Varanus

Herpetology Notes, volume 7: 723-729 (2014) (published online on 21 December 2014)
First case of conjoined twins in the Quince Monitor Lizard
Varanus melinus Böhme & Ziegler, 1997
Mona van Schingen1, 2, * and Thomas Ziegler1, 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
Cologne Zoo, Riehler Straße 173, 50735, Cologne, Germany
University of Cologne, Institut of Zoology, Department of
Terrestrial Ecology, Zülpicher Straße 47b, 50674, Cologne,
Germany
* Corresponding author e-mail: mschinge@smail.uni-koeln.de
1
2
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.
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 96605 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.
725
First case of conjoined twins in the Quince Monitor Lizard
1 Table 1: Mensural and selected meristic data of the conjoined twins (ZFMK96604), the
Table 1. Mensural
selected sibling
meristic
data of96605),
the conjoined
twins (ZFMK96604),
the malformed
siblingof(ZFMK 96605), and
2 and
malformed
(ZFMK
and a normally
developed specimen
(ZFMK 96606)
3 Varanus
melinus
compared
the type
series compared
(after Böhme
1997).
For and Ziegler 1997).
a normally developed
specimen
(ZFMK
96606) oftoVaranus
melinus
to theand
typeZiegler
series (after
Böhme
4 seeabbreviations
materialall
andmeasurements
methods; all measurements
in mm.
For abbreviations
material andsee
methods;
in mm. Bilateral
values are given as left / right.
5
6
Abbreviation
ZFMK96604a
ZFMK96604b
ZFMK 96605
ZFMK 96606
SVL
49.6
40 – 50
91.1
160.0
300 – 420
TaL
111.9
84.4
134.3
238.6
520 – 730
Type series
ToL
161.5
124.4 – 134.4
225.4
398.6
920 – 1150
A
19.8 / 20.2
17.7 / 17.6
26.3 / 24.9
31.5
48 – 67
B
10.9
9.1
14.6
16.1
21 – 30
C
7.8
6.9
10.5
12.6
16 – 22.5
G
5.0 / 4.0
4.2 / 3.5
8.2 / 7.6
8.3
13 – 20
H
5.1 / 4.7
3.2 / 3.7
7.4 /6.4
6.4
7 – 11
ElHa
14.2 / 10.9
9.3 / 9.2
-
16.4 / 16.2
-
Thorn
0.1
0.04
0.29
-
-
G/H
0.98 / 0.85
1.3 / 0.95
1.1 / 1.2
1.3
1.67 – 1.86
A/B
1.82 / 1.85
1.95 / 1.93
1.8 / 1.7
1.96
2.23 – 2.39
A/C
2.54 / 2.59
2.57 / 2.55
2.5 / 2.4
2.5
2.75 – 3.06
P
47
42
43
42
46 – 55
Q
81
64
69
81
81 – 85
R
50
50
52
58
58 – 68
S
98
-
144
126
124 – 130
T
90
56
90 / 69
90
87 – 99
N
56
49
80 / 73
84
86 – 89
AG
67 / 68
56 / 29
88 / 60
105 / 105
-
TN (=T+N)
146
105
170 / 142
174
173 – 187
X
36 / 12
36 / 22
52 / 38
40.7
29 – 45
c
27 / 25
16 / 22
26 / 25 – 26
25
27 – 30
Sub
27 / 25
13 / 21
25 / 26
25 / 26
-
M
100
68
104
86
83 – 90
U
5/4
3/4
0/2
4–5/5
-
7
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
1
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
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
124–130). 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 (105–146 versus 173–187), 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 67–68 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.
727
First case of conjoined twins in the Quince Monitor Lizard
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. 10.9
mm on the right, see Table 1).
Description of the malformed hatchling (ZFMK
96605)
The vertebral column of ZFMK 96605 (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 96605 furthermore
differs in the following characters: notched tail base and
thus less scales around tail base (69 vs. 81–85); a greater
number of scales around the midbody (144 vs. 124–130)
and a lower number of ventral scales on the right body
side (170 left, 142 right vs. 173–187 ventral scale rows
from snout to insertion of hind limbs). Furthermore,
ZFMK 96605 dorsolaterally shows a thorn-shaped
formation of scales on the right side, pointing to the
dorsolateral fold.
Both hemipenes of ZFMK 96605 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 40–50 mm versus 109–116 mm, see Ziegler
et al., 2010). Also the malformed individual ZFMK
96605 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 96605 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.
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 96605 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
Mona van Schingen & Thomas Ziegler
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.
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Accepted by Christoph Liedtke