Module 3. Lizards and Amphisbaenids

3.1

The Spinosaurus was a carnivorous reptile that lived approximately 97-112 million years ago during the Cretaceous Period in what is modern-day North Africa [1]. A prominent feature of the species, which lends to its name, is the sail on its back composed of long spines and tissue [1]. It is thought this sail was used both for thermoregulation and for use in displays to attract mates [1]. A comparison can be drawn between the sail on Spinosaurus and the sail on the modern-day Hydrosaurus pustulatus, also known as the Sail-fin lizard [2]. The Sail-fin lizard is native to the Philippines and it is thought that its sail is used for both thermoregulation and mating displays, as is thought with Spinosaurus [2]. Of interesting note is that the sail on the Sail-fin lizard is thought to be used for propulsion in water, it is known that Spinosaurus lived on land and in water and it is possible that it was used in similar circumstances for the same reason [1,2]. The few recovered bones and vertebrae of Spinosaurus indicate that it had a snout very similar to that of modern-day crocodiles, not only that but it also had similarities in its eating habits, with a diet consisting of fish [1].

3.2

Chameleons exhibit a fairly slow colour change which is triggered for various reasons. Previously it was believed to be it can offset by changes in the background colour of their environment and to external stresses on the animal [3]. New research, however, indicates that the ability to colour change evolved through a need to communicate social signals without compromising the individual to potential predators [4]. According to the study led by Fox and Moussalli, the ability of the chameleon to change colour is inconsistent with the variation in environmental backgrounds indicating that the ability evolved as a means to signal socially, as opposed to the theory of it being for camoflauge [4]. The actual process of colour change is controlled by pigment cells within the dermal skin layer of the chameleon, known as chromatophores. Three different types of chromatophores, known as melanophores, iridophores and xanthophores, combine to produce different colours [5]. For example; for a reptile to display a green coloured skin, the blue coloured iridophores and the yellow coloured xanthophores must combine [5].

3.3

The skinks represent one of the largest groups of lizards, with in excess of 600 species to the family [3]. Despite the fact that there is a large number of species within the family, the skinks do not display much diversity within their group [3]. The Stump-tailed skink, Tiliqua rugosa, is native to both Southern and Western Australia [6]. Among the largest of the skink family, the Stump-tailed skink typically weights between 600-900g with a snout to vent length of approximately 18 inches [6,7]. As can be seen in Fig.1, Stump-tailed skinks typically have rough, irregular scales and they possess a blue coloured tongue which is used primarily as a sensory organ [6]. Viviparous by nature, Tiliqua rugosa will form monogamous pairings approximately 8 weeks prior to mating. Couples will part shortly after mating but reunite the next year. One study observed a pair of the lizards pairing for ten consecutive years, indicating not only monogamous behaviour but recognition ability [6,7,8]. The female of the species will gestate for approximately 5 months with young being produced in early Spring [6]. Tiliqua rugosa are typically omnivores, feeding on a variety of vegetation and supplementing the diet with arthropods and carrion [6].

3.4

a) Parthenogenesis is a form of asexual reproduction displayed in some species of reptile where the genetic information of a male is not required and clonal offspring will be genetically identical to their mother [5]. Parthenogenesis, and asexual reproduction in general, are disadvantageous in that genetic variation among individuals is close to non existent. If environmental conditions develop so as to have a negative impact on individuals of the genotype, the genotype as a whole will suffer due to the inescapable fact they are genetically identical and therefore identically susceptible to external environmental factors [5,9].

b)In sexual reproduction a female only contributes half of the genetic material, requiring the implementation of a male genome to reproduce [5]. In comparison to asexual reproduction, sexual reproduction will not produce populations quite so quickly due to the fact individuals must find each other, court and with mate with successful fertilisation [5,9]. There is  the potential for positive traits from an individual to be lost to future generations due to the fact only half their genetic information is being used [5].

3.5

Any post-ovipositional behaviour that increases survivability of offspring whilst requiring effort by the parent, can be described as parental care [5]. There are several methods by which reptiles will care for their young; a parent may actively guard young after their young hatch so as to ensure that they survive, as is the case with Leptodactylus ocellatus, the female of which will guard her tadpoles and attack intruders [5].  Directly feeding the young is another example of parental care, the female Anotheca spinosa will lay unfertilised eggs for the tadpoles to consume [5]. Transporting the young is another way that parents will care for them, crocodiles such as Crocodylus palustris will carry its young to the waters edge in their mouths. Likewise some species of frog will carry their young froglets on their backs until they have developed further [5]. Prior to hatching, an adult may also attend the nest site to ensure the safety of the eggs. Salamanders, frogs and crocodylians are all known to engage in active nest guarding [5]. Egg brooding is another form of parental care but one which is carried out differently by amphibians and reptiles. Amphibians will tend to transport their eggs/larvae from their nest site to an aquatic site whilst reptiles will keep their eggs in a land-based nest where they will actively guard them [5]. Advantages of parental care are that eggs and larvae are kept safe from predators and environmental factors meaning that their chances of safe development and survival are increased, if a parent is actively fending off intruders there is less potential for predators to attack eggs and larvae [5]. Whilst brooding a parent will use its own body heat to raise the temperature of its eggs, resulting in faster development of embryos [5].  Behaviours such as feeding young ensures proper nutrition is received contributing to proper development [5]. The disadvantages of parental care are that in all instances the parents are not only using vital energy but actively placing themselves in harms way. A reptile that is brooding is effectively tied to the position of the terrestrial nest and must either successfully fend off intruders or succumb to predators itself [5].

3.6

Symbiosis can be described as an association between two or more organisms of a different species [9,10]. Whilst some symbiotic relationships benefit all the organisms involved, some relationships benefit only one organism with one or more organisms being left unaffected [10]. An example of a mutually beneficial symbiotic relationship is that of the ocellaris clownfish which makes its home amidst the stinging tentacles of sea anemones, the clownfish protects the anemone from predators whilst the anemone does the same in turn [10,11,12]. Commensaltic relationships involve one organism benefiting from another but not harming it in the process, an example is the relationship between hermit crabs and gastropod shells, the hermit crabs use the shells as protection but the gastropod shells are not harmed in the process [10,11]. Not all symbiotic relationships are beneficial to organisms involved, parasitic relationships often subject one or more organisms to negative effects. Necrotrophic parasites will kill their host whilst biotrophic parasites rely on their host remaining alive [10].

3.7

The Australian thorny devil, Moloch horridus, is native to the sandy deserts of inland Australia and renowned for the large, boneless spines that cover its body [13,14]. The thorny devil’s diet consists entirely of ants, in particular ants belonging to the genera Iridomyrmex such as Iridomyrmex rufoniger [13,14].  The thorny devil is what is known as a sit and wait predator, it typically will wait in areas where it can feed on ants as they move past in terrestrial and vegetation trails [13,14]. Thorny devils eat approximately 750 ants a day and have large stomachs to ensure they can hold a good amount of ants. It is necessary for them to ingest so many ants due to the fact ants are primarily chitinous [13,14].

3.8

The Komodo dragon, Varanus komodoensis is native to the Lesser Sunda Islands of Indonesia, the heaviest lizard on the planet, the Komodo dragon can weigh 366 pounds and can grow up to approximately 10.3 feet in length [15,16]. The Komodo dragon is part of the monitor family and as such it is an active lizard. As the apex predator of the islands they inhabit,Komodo dragons will hunt all sizes of prey including water buffalo, sitting in wait and then springing to attack using their serrated teeth and claws to kill [5,15,16]. Komodo dragons are also active scavengers feeding off of carrion. It is interesting to note that a Komodo dragon’s saliva is riddled with in excess of 50 strains of bacteria and that they also possess venom glands in their jaw, if a Komodo dragon fails to kill its in prey in an initial attack it will follow using its keen sense of smell, waiting until the prey eventually succumbs to the bacterial/venomous bites [15,16,17,18]. It was initially believed that the bites inflicted by the Komodo dragon were subsequently made infectious by its bacteria ridden saliva but recent research contests that the venom glands in the jaw play a more significant role, preventing blood clotting and inducing shock [17,18].

Komodo dragons display little sexual dimorphism, apart from a slight variation in scale arrangement around the cloaca [16]. The mating season for Komodo dragons is typically between May and August, males will wrestle each other for the opportunity to mate with females with eggs being laid in terrestrial nests around September [16,17]. Juveniles hatch after around nine months of incubation. Once hatched juveniles are extremely vulnerable, there is no evidence to suggest that Komodo dragons provide parental care, young Komodo dragons will feed on small rodents, snakes and lizards and inhabit wooded areas [16,17,19]. It is necessary to mention that Komodo dragons have exhibited the ability for asexual reproduction, parthenogenesis, in captive environments. Research suggests that this is almost a “last resort” and utilised when sexual reproduction is not viable [20].

3.9

The common basilisk, Basiliscus basiliscus, are found throughout South America, from Nicaragua to Columbia [21]. The common basilisk is largely terrestrial, inhabiting lowland forests with close access to water [22]. Common basilisk do make good climbers and will inhabit trees often towards nightfall [22]. Common basilisk are omnivores, feeding on a variety of food items such as eggs, fish and arthropods [23]. Common basilisk are typically brown or dark green coloured with yellow bellies, males typically have large crests adorning their bodies [23,24]. Females will lay eggs approximately eight times a year in terrestrial nests, afterwards no parental care is given [24]. Commonly referred to as the ‘Jesus Christ Lizard’, the common basilisk will flee when predators approach, often towards water sources where it gains enough momentum that its large hind feet allow it to cross water for brief distances, using its tail as a counter balance [24,26]. Typically younger basilisks can run greater distances across water than older basilisk [24,25]. Common basilisks also possess a row of scales on their feet that they keep rolled up on land but extend for running across water, so as to increase the surface area of their feet [24].

3.10

The Florida worm lizard, Rhineura floridana, much like most of the 133 species of worm lizard, is limbless and subterranean [5,27]. The Florida worm lizard has a wormlike appearance with rings of rectangular scales encircling the body and tail [5]. The Florida worm lizard makes its home in soils that can be easily burrowed into, sandy soils preferably [28]. The species has a preference for habiting areas under leaf-mold layers [28]. The Florida Worm lizard is intolerant to moist conditions and requires dry soils to inhabit [29]. Due to the fact that Florida worm lizards rarely come above ground, in captivity, it would be prudent to keep them in an enclosure with a substrate of loose, sandy soil and a top layer of leaf litter [29]. As Florida worm lizards, like other amphisbaenids, likely make a habit of laying eggs beneath the soil, this would make it even more necessary to have a substrate for the worm lizard to burrow into [28,29].

Module Project

a)

Comparison of the Iberian worm lizard, Blanus cinereus, and the Bedrigai’s Skin, Chalcides bedriagai.

Iberian worm lizard Blanus cinereus Bedriagai’s Skink Chalcides bedriagai
Habitat and Ecology Both species inhabit loose, sandy soils that allow burrowing [30,31].
Population The population of the Iberian worm lizard is classified as stable [30]. The population of the Bedriagai’s Skink is classified as decreasing [31].
Range Both species are endemic to the Iberian peninsula of Spain [30,31].
Reproduction Females will lay a single egg [30]. Females give birth to up to four fully formed live young [31].
Major threats Both species are threatened in the wild by increasing populations of a mutual predator, the Wild Boar, Sus scrofa [30,31].
Appearance Iberian worm lizards are a pinky-purpley colouration. They have no discernible limbs and very small eyes.  They are covered in bands of rectangular scales [32]. Ranging from brown to olive green in colouration, the Bedriagai’s Skink has smooth scales that cover its body much like a snake [33].
Body Shape Both species have a worm-like body shape, with smooth scales covering them [32,33].
Limbs The Iberian worm lizard has no discernible limbs [32]. The Bedriagai’s Skink has four short limbs [33].

b)

There are several complications that arise from keeping Komodo dragons in captive environments –

Enclosure Design

A creature as large as a Komodo dragon requires a lot of space to replicate that which it would occupy in the wild, as an example, the enclosure that houses the Komodo dragons at Colchester Zoo is 30 metres by 10 metres, an enclosure size that does not come cheaply [34]. With an enclosure built, it is necessary to furnish the enclosure so as to mimic the environment that a Komodo dragon would experience in the wild. Substrates of sand, soil and wood mulch are laid down. Not only is this natural to the Komodo dragon but it encourages natural behaviours such as burrowing [34]. It is also necessary for an enclosure to allow enough natural light, so that the Komodo dragons can get the D3 rays they require [34]. Underfloor heating lamps and methods for creating a stable humidity (such as a fog machine or spraying of tepid water) are also necessary and expensive, as an example the Komodo dragon enclosure at Chester Zoo cost £620,000 to complete [34,35].

Animal Enrichment

Being hunters and scavengers requires that Komodo dragons be active, unfortunately this necessity to be active is lost in captivity where a Kodak dragon’s sustenance is provided for it [5,15,16]. To ensure that whilst in captivity a Komodo dragon is keep active it is necessary to find methods of animal enrichment, activities such as scent trails and digging trails have shown to increase the activity and behaviours such as climbing and swimming [36]. This ensures that the captive environment is similar to the natural and that natural behaviours are being encouraged [36]. A study found that scent trails encouraged the most activity, possibly due to the Komodo dragons nature as a hunter [36].

Safety

With their innate ability to kill, it is necessary that zoo keepers are trained properly and that enclosures are designed in such a way that a “hands-off” approach can be taken to keeping, which is common practice with modern-day zoos [5,15,16,34,35]. Enclosures are designed in such a way that they are operated from areas outside, with “airlock” style door locking to ensure both the safety of the keepers and the animals [34,35].

Reproduction

Without access to males, it was discovered that in captive environments females will reproduce via parthenogenesis [37]. Without the need for a mate, parthenogenesis can result in large clutches of eggs very quickly [5,9]. Whilst this is good for the Komodo dragons, this is a difficult situation for zoo keepers, as it means that they must have the resources to incubate and house greater numbers of Komodo dragons.

In summary the difficulties of keeping Komodo dragons in captivity largely lie with having the necessary resources to provide an adequate environment that is true to their natural environment. Not only this but great care must be taken to ensure safety protocols are followed and that Komodo dragons are being provided enough enrichment that their behaviour is similar to their natural behaviours of hunting and scavenging [34,35].

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[2]             Arkive Sail-fin lizard [Online]. Available from: www.arkive.org [Accessed 24th February 2013].

[3]             Hatley, J. The Observer’s Book of Zoo Animals. Frederick Warne & Co Ltd. 1972.

[4]             Stuart-Fox, D & Moussalli, A. Selection for Social Signalling Drives the Evolution of Chameleon Colour Change. PloS Biol 6(1): e25.                   2008.

[5]             Vitt, L.J. & Caldwell, J.P. Herpetology: An Introductory Biology of Amphibians and Reptiles. Academic Press. 2009.

[6]             Animal Diversity Web Tiliqua rugosa [Online]. Available from: www.animaldiversity.ummz.umich.edu [Accessed 24th February 2013].

[7]             Vitt, L., R. Pianka. Lizard Ecology. NJ: Princeton University Press. 1994.

[8]             Bull, C.M. & Pamula, Y. Enhanced vigilance in monogamous pairs of the lizard, Tiliqua rugosa. Behavioural Ecology. 9 (5). pp.452-455.             1998.

[9]             Alters, S. Biology: Understanding Life. Jones and Bartlett Publishers, Inc. 2000.

[10]           Biology Nation. Introduction to Symbiosis [Online]. Available from: www.biology-nation.com [Accessed 12th March 2013].

[11]           Dimijian, G.G. Evolving together: the biology of symbiosis, part 1. Proc (Bayl Univ Med Cent). 13 (3). pp.217-226. 2000.

[12]           Lee, J. Amphiprion percula [Online]. Available from:   http://animaldiversity.ummz.umich.edu/site/accounts/information/Amphiprion_percula.html [Accessed 12th March 2013].

[13]           Pianka, R. Australia’s Thorny Devil [Online]. Available from: uts.cc.utexas.edu/~varanus/moloch.html [Accessed 12th March 2013].

[14]           Animal Diversity Web Moloch horridus [Online]. Available from: www.animaldiversity.ummz.umich.edu/accounts/Moloch_horridus   [Accessed 12th March 2013].

[15]           National Geographic Komodo Dragon [Online]. Available from: www.animals.nationalgeographic.co.uk/animals/reptiles/komodo-dragon/

[Accessed 14th March 2013].

[16]           Smithsonian National Zoological Park Komodo Dragon [Online]. Available from:            www.nationalzoo.si.edu/animals/reptilesamphibians/facts/factsheets.komododragon.cfm [Accessed 14th March 2013].

[17]           Arkive Komodo dragon [Online]. Available from www.arkive.org [Accessed 14th March 2013].

[18]           Fry, B.G. et al. A central role for venom in predation by Varanus komodoensis (Komodo dragon) and the extinct giant Varanus (Megalania)        priscus. PNAS. 106. 22. 8969-874. 2009.

[19]           Burnie, D. Animal. Dorling Kindersley. London. 2001.

[20]           Watts, P.C. et al. Parthenogenesis in Komodo dragons. NATURE. Vol. 444. 21/28. 2006.

[21]           Leenders, T. A Guide to the Amphibians and Reptiles of Costa Rica. Miami, Florida: Distribudores Zona Tropical, S.A. 2001.

[22]           Animal Diversity Web Common basilisk [Online]. Available from: www.animaldiversity.ummz.umich.edu [Accessed 14th March 2013].

[23]           BioExpedition Common basilisk [Online]. Available from: bioexpedition.com/common/basilisk [Accessed 14th March 2013].

[24]           WAZA Common basilisk [Online]. Available from: www.waza.org [Accessed 14th March 2013].

[25]           Glasheen, J.W. & McMahon T.A. Size-dependance of water-running ability in basilisk lizards (Basiliscus basiliscus). J Exp Bio. 199. 2611-2618. 1996.

[26]           National Geographic Jesus Christ Lizard [Online Video]. September 7th 2007. Available from:

http://www.youtube.com/watch?v=45yabrnryXk [Accessed 14th March 2013].

[27]           Crump, M. Amphibians, Reptiles, and their Conservation. Linnet Book; North Haven, Connecticut. 2002.

[28]           IUCN Red List Rhineura floridana [Online]. Available from: www.iucnredlist.org [Accessed 14th March 2013].

[29]           Empire of the Turtle Rhineura floridana [Online]. Available from: www.empireoftheturtle.com [Accessed 14th March 2013].

[30]           IUCN Red List Blanus cinereus [Online]. Available from: www.iucnredlist.org [Accessed 15th March 2013].

[31]           IUCN Red List Chalcides bedriagai [Online]. Available from: www.iucnredlist.org [Accessed 15th March 2013].

[32]           NaturePhoto-CZ Iberian worm lizard [Online]. Available from: www.naturephoto-cz.com [Accessed 15th March 2013].

[33]           Herpetofauna of Europe Herpetological trip to Andalucia and Murcia (southern Spain) 14th of April – 30th of April 2006 [Online]. Available

from: www.hylawerkgroep.be [Accessed 15th March 2013].

[34]           Colchester Zoo Enclosure design [Online]. Available from: www.colchester-zoo.com [Accessed 15th March 2013].

[35]           ZooLex Islands in Danger [Online]. Availble from www.zoolex.org [Accessed 15th March 2013].

[36]           Veasley, J.A. & Guerra, G. Environmental Enrichment for Captive Komodo Dragons [Online]. Available from www.cfr.washington.edu

[Accessed 15th March 2013].

[37]           BIAZA Parthenogenesis in Komodo Dragons [Online]. Available from: www.biaza.org.uk [Accessed 15th March 2013].

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