Animals walking on walls: challenging gravity

How do insects, spiders or lizards for walking on smooth vertical surfaces or upside down? Why would not be possible for Spiderman to stick on walls the way some animals do?

Scientist from several areas are still in search of the exact mechanisms that allow some animals to walk on smooth surfaces without falling or sliding. Here we bring you the latest discoveries about this topic.

Competition for space and resources (ecological niche) has led to a lot of amazing adaptations throughout the evolution of life on Earth, like miniaturization.

When nails, claws or friction forces are insufficient to climb up vertical smooth surfaces, dynamic adhesion mechanisms come into play. Dynamic adhesion mechanisms are defined as those that allow some animals to climb steep or overhanging smooth surfaces, or even to walk upside down (e.g. on ceilings), by attaching and detaching easily from them. The rising of adhesive structures like adhesive pads as an evolutionary novelty has allowed some animals to take advantage of unexplored habitats and resources, foraging and hiding from predators where others could not.

Gecko stuck on a glass surface. Picture by Shutterstock/Papa Bravo.

Adhesive pads are found in insects and spiders, some reptiles like geckos and lizards, and some amphibians like tree frogs. More rarely they can be also found in small mammals, like bats and possums, arboreal marsupials native to Australia and some regions from the Southeast Asia.

The appearance of adhesive pads among these very different groups of animals is the result of a convergent evolution process: evolution gives room to equal or very similar solutions (adhesive pads) to face the same problem (competence for space and resources, high predation pressure, etc.).

Adaptation limits (or why Spiderman could not climb up walls)

Studying the underlying processes of the climbing ability of these animals is a key point in the development of stronger adhesive substances. So, a lot of research regarding this topic has been carried out to date.

Will humans be able to climb up walls like Spiderman some day? Labonte et al. (2016) explain us why Spiderman could not be real. Or, at least, how he should be to be able to stick on walls and do whatever a spider can.

Will humans be able to climb up walls like Spiderman some day? For now, we will have to settle for this sculpture. Public domain image.

Apart from the specific mechanisms of each organism (of which we will talk in depth later), the main principle that leads the ability for walking on vertical smooth surfaces is the surface/volume ratio: the smaller the animal, the larger is the total surface of the body with respect its volume and smaller is the amount of adhesive surface needed to avoid falling due to the body weight. According to this, geckos are the bigger known animals (i.e. those with the smallest surface/volume ratio) able to walk on vertical smooth surfaces or upside down without undergoing deep anatomical modifications.

And what does ‘without undergoing deep anatomical modifications’ mean? The same authors say that the larger the animal, the bigger is the adhesive pad surface needed for walking without falling to the ground. The growth of the adhesive pad surface with respect the size of the animal shows an extreme positive allometry pattern: by a small increase of the animal size, a bigger increase of the adhesive pad surface takes place. According to this study, a 200-fold increase of relative pad area from mites to geckos has been observed.

Picture by David Labonte

However, allometry is led by anatomical constraints. Therefore, if there was an animal larger than a gecko able to climb up smooth surfaces, it should have, for example, extremely large paws covered by an extremely large sticky surface. While this would be possible from a physical point of view, anatomical constraints would prevent the existence of animals with such traits.

Now we are in condition to answer the question ‘Why Spiderman could not stick to walls?’. According to Labonte et al., to support a human’s body weight, an unrealistic 40% of the body surface would have to be covered with adhesive pads (80% if we only consider the front of the body) or ridiculously large arms and legs should be developed. Both solutions are unfeasible from an anatomical point of view.

Great diversity of strategies

Dynamic adhesion must be strong enough to avoid falling as well as weak enough to enable the animal to move.

A great diversity of dynamic adhesion strategies has been studied. Let’s see some of the most well-known:

Diversity of adhesive pads. Picture by David Labonte.

1) Wet adhesion

A liquid substance comes into play.

Insects

Insects develop two main mechanisms of wet adhesion:

Smooth adhesive pads: this mechanism is found in ants, bees, cockroaches and grasshoppers, for example. The last segment of their legs (pretarsus), their claws or their tibiae present one or several soft and extremely deformable pads (like the arolia located in the pretarsus). No surface is completely smooth at microscale, so these pads conform to the shape of surface irregularities thanks to their softness.

Cockroach tarsus. Adapted picture from the original by Clemente & Federle, 2008.

Hairy adhesive pads: these structures are found in beetles and flies, among others. These pads are covered by a dense layer of hair-like structures, the setae, which increase the surface of the leg in contact with the surface.

Chrysomelidae beetle paw. Picture by Stanislav Gorb et al.

A thin layer of fluid consisting of a hydrophilic and a hydrophobic phase located between the pad and substrate comes into play in both strategies. Studies carried out with ants show that the ends of their legs secrete a thin layer of liquid that increases the contact between the pretarsus and the surface, filling the remaining gaps and acting as an adhesive under both capillarity (surface tension) and viscosity principles.

Want to learn more about this mechanism in insects? Then do not miss the following video about ants!

Tree frogs

Arboreal or tree frog smooth toe pads are made of columnar epithelial cells separated from each other at their apices. Mucous glands open between them and secrete a mucous substance that fill the intercellular spaces. Having the cells separated enable the pad to conform to the shape of the surface and channels that surround each epithelial cell allow to spread mucus over the pad surface to guarantee the adhesion. These channels also allow to remove surplus water under wet conditions that could make frogs to slide (most tree frogs live in rainforests).

Red-eyed tree frog (Agalychnis callidryas), distributed from Southern Mexico to Northeastern Colombia. Public domain image.

In the next video, you can see in detail the legs of one of the most popular tree frogs:

Smooth toe pads of tree frogs are similar to those found in insects. In fact, crickets have a hexagonal microstructure reminiscent of the toe pads of tree frogs. This led Barnes (2007) to consider the wet adhesion mechanism as one of the most successful adhesion strategies.

Different species of tree frogs (a, b, c) and their respective epithelia (d, e, f). Figure g corresponds to the surface of a cricket’s smooth toe pad. Picture by Barnes (2007).

Possums

The most detailed studies on possums have been carried out about the feathertail glider (Acrobates pygmaeus), a mouse-sized marsupial capable to climb up sheets of glass using their large toe pads. These pads are conformed by multiple layers of squamous epithelium with alternated ridges and grooves that allow them to conform to the shape of the surface and that are filled with sweat, the liquid this small mammal use to adhere to surfaces.

Acrobates pygmaeus. Picture by Roland Seitre.

Frontal toe pads of Acrobates pygmaeus. Picture by Simon Hinkley and Ken Walker.

2) Dry adhesion

Liquid substances do not come into play.

Spiders and geckos

The adhesion of both spiders and geckos depends on the same principle: the Van der Waals forces. Unlike insects, tree frogs and possums, these organisms do not secrete sticky substances.

Van der Waals forces are distance-dependent interactions between atoms or molecules that are not a result of any chemical electronic bond. These interactions show up between setae from footpads of geckos (which are covered by folds, the lamellae) and setae from spider paws (which are covered with dense tufts of hair, the scopulae), and the surface they walk on.

Spider paw covered with setae. Picture by Michael Pankratz.

Diversity of footpads of geckos. Picture by Kellar Autumn.

However, recent studies suggest dry adhesion in geckos is not mainly lead by Van der Waals forces, but by electrostatic interactions (different polarity between setae and surface), after confirming that their sticking capacity decreased when trying to climb a sheet of low energetic material, like teflon.

Anyway, the ability of geckos to climb is impressive. Check this video of the great David Attenborough:

3) Suction

Bats

Disk-winged bats (family Thyropteridae), native to Central America and northern South America, have disk-shaped suction pads located at the base of their thumbs and on the sole of their feet that allow them to climb smooth surfaces. Inside these disks, the internal pressure is reduced, and the bat stick to the surface by suction. In fact, a single disk can support the weight of the bat’s body.

Thyropteridae bat. Picture by Christian Ziegler/ Minden Pictures.

Now that you know about all these animals’ ability for climbing smooth walls, do you still think Spiderman is up to the task?

Main picture by unknown author. Source: link.

Colour change in chamaleons: an emotional rainbow

Many people consider chameleons to be the masters of camouflage. Their ability to change colour leads us to believe that these animals have evolved to blend in with their surroundings and to trick their predators. But, what would you think if I told you that camouflage isn’t the main reason for colour shifts in chameleons? In this new entry, apart from explaining how chameleons change their coloration, we’ll show you how these cryptic animals use colour change for a wide array of reasons.

MYTHS ABOUT CHAMELEONS

Chameleons (Chamaeleonidae family) are extremely cryptic lizards, as their coloration is usually very similar to that of their habitat’s. Also, many chameleon species present the ability to actively shift their colours, making their camouflage even more complex.

Usambara soft-horned chameleon female (Kinyongia tenuis) displaying striking colouring. Photo by Keultjes.

There is much misunderstanding regarding chameleons’ colour changing abilities. Here you have some refuted myths about chameleons:

• The different chameleon species can only change into a limited range of colours.
• Chameleons do not change their coloration rapidly, as they do it subtly. If they did, they would be much easier to spot by their predators.
• Chameleons don’t change their colours depending on what they are touching but, as we’ll see below, their reasons are much more complex.

Video from Viralweek which gives a wrong idea about how a veiled chameleon changes its colours (Chamaeleo calyptratus).

But, how do chameleons change their colours? Many other animals, like cephalopods and some fish and lizards, also have the capacity to shift colours. In most cases it is achieved using chromatophores, a type of pigmentary cell found on ectothermic animals. In colour-changing animals, chromatophores are distributed in multiple layers and have the ability to contract, expand, aggregate or disperse, causing different colour variations.

Detail of a cuttlefish chromatophores, by Minette Layne. Depending on whether they contract or expand, different colours can be appreciated.

For a long time it was thought that chameleons changed their colours using only their chromatophores. But a recent study showed that chameleons bring colour change to the extreme. This study was being conducted by a team of biologists and physicists when they noticed something special: chameleons do not present any green pigment in their skin!

PIGMENTS AND CRYSTALS

In order to explain how chameleons change colours, first we must distinguish between two different kinds of coloration in animals: pigmentary and structural colour. Pigmentary colour is the commonest, as it’s the one that an organism presents due to pigments present in their tissues (such as melanin in human skin). Instead, as we explained in a former article, structural colour is generated by the refraction of light with some skin microstructures.

Image of an upside down beetle in which various structural colours can be seen. Photo by David López.

And what happens with chameleons? Well, it’s a combination of both mechanisms. Chameleons present black, red and yellow chromatophores, which they can contract and expand voluntarily. Also, in a study conducted with panther chameleons (Furcifer pardalis), it’s been proved that they also present two layers of guanine nanocrystal-bearing cells, called iridiophores, which reflect light. Then a chameleon’s green coloration is acquired by the blue light reflected by the iridiophores that goes through the outer yellow chromatophores.

Scheme of a chameleon’s skin section in which the iridiophores (blue) with nanocrystal layers and the different kinds of chromatophores can be seen; xanthophores (yellow), erythrophores (red) and melanophores (black). Image by David López.

Chameleons also present a series of neural circuits that allow them to control de composition and the distance between the iridiophores’ nanocrystals in different parts of their skin. This allows them to control the wavelength of the light reflected by the iridiophores and so, the colour. Combined with the chromatophores, the different chameleon species can cover most of the visible spectrum of colours.

Differences in the colouring of a panther chameleon when it’s relaxed and excited, and its relation with the composition and distribution of the iridiophore nanocrystals. Image extracte from Teyssier & Saenko.

CHANGING COLOURS FOR WHAT?

Even if there are other squamosal species that can shift colours, this usually is because of a physiological response to thermoregulation, excitement or changes related to reproduction. Chameleons, also have an important part of their nervous system dedicated to changing colour rapidly, consciously and reversibly. They can even change different skin regions to different colours and, while one region becomes more orange or red, another one becomes more bluish or whitish, creating pretty striking colour effects and contrasts.

But then, why do chameleons change their colours? Well, the truth is that the kaleidoscopic abilities of these lizards have different functions, varying among the different species.

CAMOUFLAGE

The most obvious motive (even if not the most important) is camouflage. Even if the standard coloration of most chameleon species is cryptic enough, in case of necessity chameleons are able to blend in even more with their surroundings. This helps them not to be detected by their prey, but mainly to go unnoticed by their predators.

Mediterranean chameleon (Chamaeleo chamaeleon) perfectly blending in with its surrounding. Photo by Javier Ábalos Álvarez.

Also, in a study conducted with Smith’s dwarf chameleons (Bradypodion taeniabronchum), is was proved that these were able to adjust the degree of their colour shifts to the visual capacities of their predators. Birds and snakes both feed on chameleons but, while the former have a great perception of shapes and colours, the latter doesn’t have such a sharp vision. It’s seen that Smith’s dwarf chameleons show more convincing colour changes when faced with a predator bird, than they do when faced with a snake.

Photos of a Smith’s dwarf chameleon blending in when facing two decoy predators, a shrike and a mamba. Photo by Devi Stuart-Fox.

THERMOREGULATION

Chameleons are ectothermic and, like most reptiles, depend on external sources of heat. Apart from the more superficial iridiophores (called S-iridiophores), chameleons have a deeper layer of iridiophores called D-iridiophores, which (even if they present a much messier nanocrystal structure that cannot be modified) highly reflect infrared light, and it is thought that they must have some thermoregulation-related function. Many other lizards also present an iridiophore layer similar to D-iridiophores.

Apart from D-iridiophores, chameleons also shift to darker or lighter colours in order to regulate their body temperature. This becomes more apparent in species that live in habitats with more extreme climates. As we explained in an earlier entry, the Namaqua chameleon (Chamaeleo namaquensis), which inhabits deserts in south-western Africa, presents an almost black colour during the early morning hours, in order to absorb the maximum heat, while during the hottest hours it shows a whitish coloration, in order to reflect the maximum solar radiation.

Two different coloration patterns in a Namaqua chameleon, a lighter one (photo by Hans Stieglitz) and a darker one (photo by Laika ac).

COMMUNICATION

The main function of chameleons colour change is intraspecific communication. Chameleons use different colour patterns known as liveries in some countries, which are changed in order to transmit information to other individuals of their same species like their stress degree, their reproductive or health status, etc… A chameleon’s standard coloration is usually similar to that of their habitat. So, this colour pattern usually indicates a healthy animal, while if they feel sick or have some physical problem, they usually present paler and duller colorations.

Dominance and submission patterns on three dwarf chameleon species (Bradypodion sp.) Image from Adnan Moussalli & Devi Stuart-Fox.

In many species, females present more conspicuous and contrasted patterns when they are in heat, while they show a darker coloration after mating. When seeing these signals, males know which females are available and with which females they should better save their energy. Males also present more eye-catching patterns during the mating season, in order to indicate their intentions to females and to warn their rivals.

Female carpet chameleon (Furcifer lateralis) with a pattern that indicates that it’s already pregnant and that it has no interest in mating. Photo by Bernard Dupont.

Finally, outside mating season, all chameleons use their boldest colours during their encounters with rivals of their same species. It’s in these situations when chameleons show the most contrasted patterns, apart from inflating and looking bigger and more aggressive, in order to scare off their rivals.

Video of a panther chameleon (Furcifer pardalis) acting aggressively when presented with a “rival”. Video from The White Mike Posner.

As we’ve just seen, the variety of colorations among the distinct chameleon species is huge. Yet, their incredible abilities haven’t saved chameleons from being on the endangered species list, as many of them are in danger of extinction, mainly because of the destruction of their habitat due to the logging industry and because of poaching for the illegal exotic animal trade. We hope that with a better awareness of these spectacular and colourful lizards, future generations can still delight with chameleon colour shifts for a long time.

REFERENCES

The following sources have been consulted during the elaboration of this entry:

• Masó & Pijoan (2011). Anfibios y Reptiles de la Península Ibérica, Baleares y Canarias. Ediciones Omega.
• Teyssier, Saenko et al. (2015). Photonic crystals cause active color change in chameleons. Nature communications Vol. 6. Pp 6368.
• Stuart-Fox & Moussalli (2008). Selection for Social Signalling Drives the Evolution of Chameleon Colour Change. PLoS Biol Vol. 6.
• Ligon & McGraw (2013). Chameleons communicate with complex color changes during contests: different body regions convey different information. The Royal Society.
• Russel A. Ligon (2014). Defeated chameleons darken dynamically during dyadic disputes to decrease danger from dominants. Behav Ecol Sociobiol Vol. 68. Pp: 1007.
• New Scientist. Chameleons fine-tune camouflage to predator’s vision.
• Cover image by Tambako the Jaguar.

Tuatara: reintroduction of a living fossil

There’s a reptile in New Zealand whose lineage arose in the time of the dinosaurs. Even if its external appearance is similar to that of a lizard, the tuatara (whose name means “spiny back” in the Maori language) is an animal with many unique characteristics that classify it in an order different from the other reptiles. In this entry we’ll explain the main characteristics of this relic from the past, as interesting as endangered.

ORIGIN AND EVOLUTION

The tuataras are unusual reptiles whose lineage goes back to 240 million years ago, at the middle Triassic. Tuataras are lepidosaurs, yet they form a different lineage from the squamates, and that’s why they are found in their own order, the rhynchocephalians (order Rhynchocephalia). Lots of species flourished during the Mesozoic, even if almost all of them were replaced by squamates. At the end of the Mesozoic only one family survived, the Sphenodontidae.

Homoeosaurus fossil, an extinct relative of the tuataras. Photo by Haplochromis.

Of all the existing sphenodontids, only tuataras have survived to the present day. Traditionally it was considered that tuataras included two species: the common tuatara (Sphenodon punctatus) and the Brother’s Island tuatara (Sphenodon guntheri), although recent analyses have popularized the idea that the tuatara is only one species, S. punctatus.

TUATARA ANATOMY

As we have already stated, tuataras look externally like a lizard, having a certain resemblance to iguanas. Male tuataras are larger than females, measuring up to 61 cm in length and one kilogramme of weight, while females only measure 45 cm and weigh half a kilo. Tuataras present a spiny crest on their backs which give them their common name. This crest is bigger in males, and can be erected as display.

Photo by KeresH of a young male tuatara.

What really distinguishes the tuataras is their internal anatomy. All the other reptiles have modified greatly their skull structure, but tuataras have maintained the original diapsid configuration without most changes. While crocodiles and turtles have developed a sturdy skull, tuataras conserve wide temporal openings, and while squamates have developed flexible skulls and jaws, tuataras keep a rigid cranium. Also, unlike most reptiles, tuataras present no external ears.

Modified image from the drawing by Nobu Tamura of the tuatara skull. In it we can see the main characteristics that distinguish it: 1. Beak-shaped premaxilla, 2. Acrodont teeth, fused to the jaws, 3. Diapsid-like wide temporal openings and 4. Parietal or pineal opening.

The name Rhynchocephalia means “beak head” and it refers to the beak-like structure of their premaxilla. Tuataras are also one of the few reptiles with acrodont teeth, which are fused to the maxilla and the jaw, and are not renewed. Also, they present a unique saw-like jaw movement, moving it forwards and backwards.

Video by YouOriginal, of some captive tuataras feeding. In this video we can appreciate the singular jaw movement.

Finally, one of the more incredible anatomic characteristics of tuataras is that they conserve their parietal or pineal eye. This is a structure reminiscent from the first tetrapods, which connects with the pineal gland and which is involved in the thermoregulation and circadian rhythms. Even if some other animals also keep it, the tuataras present a real third eye, with complete lens, cornea and retina, even if it gets covered with scales as they age.

HABITAT AND BIOLOGY

Tuataras live in some thirty islets in the Cook Strait, between the two main islands of New Zealand. Also, the previously considered species S. guntheri is found on Brother’s Island, in the northwest of South Island. All populations live in coastal forests or scrublands, with loose soils easy to dig. Also, in most of their distribution area there are colonies of sea birds, whose nests are also used by tuataras.

Photo by Satoru Kikuchi of a typical humid forest of New Zealand.

Compared with most reptiles, tuataras live in relatively cold habitats, with annual temperatures oscillating between 5 to 28°C. Tuataras are mainly nocturnal, usually coming out of their burrows at night, even if sometimes they can be found basking in the sun during the day (especially in winter).

Tuataras have few natural predators. Apart from some introduced animals, only gulls and some birds of prey represent a danger for these reptiles. In contrast, their diet is fairly varied. Being sit-and-wait predators, tuataras feed mainly on invertebrates like beetles, crickets and spiders, even if they are able to predate on lizards, eggs and bird chicks, and even younger tuataras. As their acrodont teeth don’t renew, these get worn down in time, so older individuals usually feed on softer prey like snails and worms.

Tuataras mate between January and March (summer), when the territorial males compete for the females, which will lay around 18-19 eggs between October and December (spring). The sex of the offspring depends on the incubation temperature (males at higher temperatures and females at lower ones). The eggs will hatch after 11-16 months (one of the longest incubation periods of all reptiles), from which young tuataras will be born, who will avoid the cannibalistic adults being active mainly during the day.

Unique video of the birth of a tuatara at the Victoria University of Wellington. The translucent mark on the little tuatara’s head corresponds to the parietal eye.

As we can see based on their long incubation period, tuataras develop slowly. These reptiles do not reach sexual maturity until the age of 12, and they keep growing. Also, tuataras are extremely long-lived animals, living up to more than 60 years in the wild. In captivity they can live more than 100 years.

CONSERVATION AND THREATS

Before the arrival of man, the tuataras were present in both main islands of New Zealand and many more islets. When the first European settlers arrived, tuataras were already only found in about 32 little islands. It’s believed that the extinction of tuataras from the main islands was due to habitat destruction and to the introduction of foreign mammals like rats. Other threats include the low genetic diversity caused by isolation of the different populations and climate change, which can affect the sex of the offspring.

Current distribution map of the tuataras. The squares correspond to the old species Sphenodon guntheri, now considered a population of S. punctatus.

When the first human settlers arrived in the isles, it is thought that 80% of New Zealand was covered in forests. When the first Polynesian tribes came around the year 1250, they caused the deforestation of more than half the archipelago. Centuries later, with the arrival of Europeans, deforestation intensified even more, up to the current situation, with only 23% of the original forest still preserved.

Photo by Cliff of a Pacific rat (Rattus exulans), one of the main threats for the tuataras.

The introduction of foreign mammals has been one of the main factors of the recent decline of tuataras, especially the introduction of the Pacific rat (Rattus exulans). This rodent has affected the populations of both tuataras and many of New Zealand’s endemic bird species. In studies on coexisting populations of tuataras and rats, it has been observed that rats, apart from preying on eggs and hatchlings, also compete with adult tuataras for resources. With an extremely slow life cycle, tuataras can’t recover from this impact.

Photo by Br3nda of a reintroduced and tagged tuatara.

Yet, tuataras are currently classified as “least concern” in the IUCN red list. This is thanks to the great efforts of conservation groups that have contributed to the recovery of this species. One of the main tasks has been the eradication of the Pacific rat from the main island where tuataras live. In order to do that, a titanic effort was made in many islets where entire populations of tuataras were captured to participate in captive breeding programs, while the rats were eliminated from these islands. After their main threat was eradicated, all the captured individuals and their captive-born offspring were released in their natural habitat so they could live without such a fierce competitor.

Video by Carla Braun-Elwert, about the breeding success of an old tuatara couple.

Currently, the wild tuatara population is estimated to be between 60.000 and 100.000 individuals. It can be said that this living fossil, which was on the brink of extinction after millions of years of existence, received a second opportunity to keep inhabiting the incredible islands of New Zealand. We hope that in the future, we can keep enjoying the existence of these reptiles, the only survivors of a practically extinct lineage, for many more centuries.

REFERENCES

The following sources have been consulted during the elaboration of this entry:

• Halliday & Adler (2007). La gran enciclopedia de los Anfibios y Reptiles. Editorial Libsa.
• Arkive. Tuatara (Sphenodon punctatus).
• The Reptile Database. Sphenodon punctatus.
• Department of Conservation, Te Papa Atawhai. Tuatara.
• Imagen de portada de Michal Klajban.

Desert reptiles

Deserts are some of the most extreme habitats on the planet. The Sahara, the Gobi and the Sonora are some examples of warm deserts where the high temperatures and the lack of water pose a great challenge to animals that live in them. Reptiles are one of the animal groups that present the most incredible adaptations for life in deserts. In this entry we’ll explain the difficulties that desert reptiles must face in order to survive, and we’ll introduce you to different species of snakes and lizards that in the deserts have found their home.

REPTILES IN THE DESERT

The characteristic which unites all deserts is the scarce precipitation as, unlike most people think, not all deserts present high temperatures (there are also cold deserts, like the Arctic and the Antarctic, both in danger because of the climate change). Reptiles thrive better in warm deserts than in cold deserts, because the low temperatures would not allow them to develop their life activity.

Map by Vzb83 of the warm deserts, both arid and semiarid, of the world.

Warm deserts not always have extremely high temperatures. While during the day temperatures may rise up to 45°C, when the sun goes down temperatures fall below freezing point, creating daily oscillations of up to 22°C. The different desert reptiles, being poikilotherms and ectotherms, use different behavioural strategies in order to avoid overheating during the day and to keep their body heat during the night (for example, climbing to elevated areas or sleeping in burrows).

The Namaqua chameleon (Chamaleo namaquensis) regulates its body heat changing its colouration. During sunrise it is black in colour in order to absorb as much radiation of the sun and activate its metabolism. When temperatures become higher, it turns white to reflect solar radiation. Video from BBC.

As we have already stated, the main characteristic of any desert is the lack of water. Generally, in a desert, it rains less than 250 mm of water a year. The scaly and impervious skin of reptiles prevents the loss of water, and their faeces contain uric acid which, compared to urea, is much less soluble in water, allowing them to retain more liquids. Most desert reptiles extract the water they need from their food and some drink water from the dew.

Both the extreme temperatures and the shortage of precipitations make the desert a place with very few living beings. Vegetation is scarce and animals are usually small and secretive. This lack of resources causes desert reptiles to be usually smaller than their cousins from more benevolent environments. Also, these saurians usually exploit any available food resource, although they think twice before wasting their precious energy to get their next meal.

SAND SNAKES

In many sandy deserts we can find various species of snakes (and legless lizards) that have adapted to a life among the dunes. Many of these ophidians share a locomotion method called “sidewinding”, in which they raise their head and neck from the ground and move them laterally while the rest of the body stays on the ground. When they place their head on the ground again they raise their body, making these snakes move laterally in a 45° angle. This method of locomotion makes these snakes move more efficiently in an unstable terrain. It also reduces the contact of their body with an extremely hot substrate, as the body of these ophidians only touches the ground in two points at a time.

As we can see in this video from RoyalPanthera, sidewinding allows desert snakes to move minimizing the contact with the hot terrain.

Many desert ophidians bury themselves in the sand both to avoid sun exposure and to blend in and catch their prey unaware. This has made many desert-dwelling snakes very sensitive to vibrations generated by their prey as it moves through the sand. In addition some species present an overly developed rostral scale (the scale at the tip of their snout), being much thicker in order to aid during excavation in sandy soils.

An example of this are the North American snakes of the Heterodon genus, also known as hog-nosed snakes, as they present an elevated rostral scale giving their snout a characteristic shape. Photo of Heterodon nasicus by Dawson.

The horned vipers of the Cerastes genus also present various characteristics that facilitate life in the deserts. These vipers evade high temperatures becoming active at night and they spend the day buried in the sand. Their hunting method consists in burying themselves waiting for a prey to pass by, this way saving most of their energy. It is believed that their horn-shaped supraocular scales cover their eyes when they are buried in order to protect them from the sand.

Photo by Tambako The Jaguar of a Sahara sand viper (Cerastes vipera), a species from North Africa and the Sinai Peninsula.

SPINY CRITTERS

In different deserts of the world we find reptiles with their bodies covered in spines. This not only provides them with certain protection against predators, but is also helps them blend in in a habitat with plenty of thorny plants. Two of these animals are members of the Iguania suborder: the thorny devil and the horned lizards.

Photo of a thorny devil (Moloch horridus) by Christopher Watson.

The thorny devil (Moloch horridus) is an agamid that lives in the Australian sandy deserts. This lizard presents spines all over its body, making it difficult for its predators to swallow. It also has a protuberance behind its head that acts as a fat storage.  When it feels threatened, it hides its real head between its legs and it exposes its neck protuberance as a decoy head. Probably, the most interesting adaptation of this animal is the system of small grooves among its scales, which collect any water that contacts its skin and conducts it directly to its mouth.

Horned lizards (Phrynosoma genus, affectionately called “horny toads”) are iguanids which are found in different arid habitats of North America. Similarly to the thorny devil, their body is covered in spines making them hard to eat for their predators. Also, when they are caught, they inflate their bodies to make the task even more difficult. Finally, some species like the Texas horned lizard (Phrynosoma cornutum) are known for their autohaemorrhagic abilities: when they feel cornered they squirt a stream of stinky blood from their eyes which scares away most predators.

Photo from the U.S. Fish & Wildlife Service of a Texan horned lizard (Phrynosoma cornutum).

As you have seen, in the deserts we can find reptiles with some of the most inventive (and disturbing) adaptations of the world. These are only a few examples of the astonishing diversity of squamates that are found in the deserts of the world, which only seek to survive the harsh conditions of these extreme environments. Sometimes, it’s just a matter to avoid burning your feet with the hot sand.

Video from BBCWorldwide of a shovel snouted lizard (Zeros anchietae) making the “thermal dance” in order to diminish the contact with the hot sand.

REFERENCES

The following sources have been consulted during the elaboration of this entry:

• Halliday & Adler (2007). La gran enciclopedia de los Anfibios y Reptiles. Editorial Libsa.
• Digital-Desert. Desert Reptiles.
• Arizona-Sonora Desert Museum. Adaptations of Desert Amphibians & Reptiles.
• In the desert. A comprehensive list of the venomous snakes found in the desert.
• H.E.R.P. Herpetological Education & Research Project.
• Christopher J. Bell, Jim I. Mead & Sandra L. Swift (2009). Cranial osteology of Moloch horridus (Reptilia: Squamata: Agamidae). Records of the Western Australian Museum. Vol 25. Pp: 201-237.
• Horned Lizard Conservation Society.
• Cover image by Yathin S. Krishnappa.

Monsters and dragons: Venomous lizards

When we think about venomous animals most people think about the same ones. Usually, we think about spiders, scorpions and snakes, despite knowing there are also venomous amphibians, fishes and mammals. Even if snakes are the best known venomous reptiles, in time we have learned that they are not the only group that present venomous glands and that many other reptiles also have the capacity of injecting venom. In this entry we’ll get to know the least known venomous saurians and we’ll try to explain their relationship with snakes.

EVOLUTION OF VENOM IN REPTILES

Everybody is familiar with the toxic abilities of snakes. Traditionally it was believed that venom evolved independently in the different groups of venomous snakes (colubrids, elapids and viperids) and in a lizard family (the helodermatids). Yet this vision has changed over the years and with the discovery of other species of venomous squamates.

The venom of many animals is used for both antivenom development and pharmacological research of analgesics and other medicines. Photo of the extraction of venom from a saw-scaled viper (Echis carinatus), by Kalyan Varma (Image under a GNU license).

Currently, it’s been shown that there are different species of saurian which present glands and organs capable of injecting venom, along with many other species with genetic material related to venom production (even if most aren’t venomous). This occurs, for example, in many apparently non-venomous snakes and lizards that retain genetic material related to the synthesis of venom. This has caused many scientists to group these reptiles under a common clade called Toxicofera, “those who bear toxins”.

This new clade includes the different squamosal taxa, which are believed to have had a venomous common ancestor. These groups are:

• Ophidia: Ophidians, snakes.

Indian wolf snake (Lycodon aulicus), example of an ophidian. Photo by Shantanu Kuveskar.

• Iguania: Iguanas, agamas and chameleons.

Brown basilisk (Basiliscus vittatus), example of an iguanian. Photo by Steve Harbula.

• Anguimorpha: Monitors, slow worms and others.

Earless monitor lizard (Lanthanotus borneensis), example of an anguimorph. Photo by Kulbelbolka.

Even though most current iguanians and anguimorphs don’t present venom, the Toxicofera theory proposes that many species would have lost their capacity to inject venom secondarily. Below we’ll present some of the lesser known venomous saurians.

MONSTERS OF THE NEW WORLD

The most famous venomous lizards are the anguimorphs of the Helodermatidae family. From their discovery it was known that these lizards where venomous, as they present a pair of venomous glands in their lower jaws and various pairs of grooved teeth similar to those of venomous snakes with which they inject venom.

Helodermatid skull, in which we can see the sharp teeth with which they inject their venom. Image from Heloderma.net.

The helodermatis are carnivorous animals which feed on small mammals, birds, wall lizards, amphibians, invertebrates, eggs and carrion. Considering its generalist diet and that their prey are pretty defenceless, it is thought that venom evolved in these reptiles as a predator deterrent method, not as a hunting strategy.

Photo by Walknboston of a Gila monster (Heloderma suspectum), in which we can see its black and yellow coloration, with which it warns its predators about its toxicity (aposematic coloration).

The Gila monster and the beaded lizard (Heloderma horridum) are slow animals which aren’t really dangerous to human beings. Yet their raising popularity as exotic pets has ended with some bite cases. The bite of a Gila monster causes some serious and burning pain, local edema, weakness, dizziness and nausea. Even if heavy bleeding is usually associated with bites, this isn’t due to some sort of anticoagulant substance but to the helodermatid’s sharp teeth and to the fact that to inject the venom they must chew their aggressor strongly , causing deep lacerations.

THE BEARDED DRAGON

The saurians of the genus Pogona are iguanians of the Agamidae family. These Australian reptiles are known as bearded dragons for the spines that they present on their throats. Even though they are adapted to live in arid places, the environmental temperature can affect the sex of their offspring.

Photo of an eastern bearded dragon in which we can see its yellow coloured mouth. Could it be that this coloration is indicating anything? Photo by Matt.

Bearded dragons are inoffensive animals, but there’s one species with a secret weapon. The eastern bearded dragon (Pogona barbata) is a venomous lizard but, while the rest of venomous reptiles only have one pair of venomous glands, the eastern bearded dragon has two pairs: two in its upper jaw and two in its lower jaw.

Transversal section of the mouth of an eastern bearded dragon, in which we can see the incipient venomous glands both in its upper jaw (mxivg) and its lower jaw (mnivg). Image extracted from Fry, Vidal et al.

The venom they produce isn’t really strong (in human beings it only causes a minor swelling) and the glands are considered vestigial. Yet, the Toxicofera theory argues that the glands of the bearded dragon show us the primitive form which the first toxicoferan reptile would have presented, with two pairs of venom glands instead of a single pair like most current venomous reptiles.

THE BIG MONITORS

Everyone has heard about monitor lizards (anguimorphs of the Varanidae family). There are hundreds of documentaries about the Komodo dragon in which we are told that these animals have so many bacteria in their mouths that their bites inflict an infection, deadly enough to kill an adult bull. Yet recent studies have shown that the monitor’s poor buccal hygiene is not what causes the death of their victims.

Perente or perentie (Varanus giganteus) a typical varanid, with long neck, strong legs, active metabolism and developed senses. Photo by Bernard Dupont.

Even if there are three frugivorous species, the rest are obligate carnivores. It has always been said that the mouth’s bacteria of the monitors is what causes the death of their prey, even if there isn’t any studies which prove it. In fact, in many studies it has been seen that the monitor’s saliva isn’t very different from that of other herbivorous reptiles.

Photo in which we see the feared monitor’s saliva, specifically from an Asian water  monitor (Varanus salvator). Image by Lip Kee.

In a study, it was demonstrated that various species of monitor lizards present venom glands in their lower jaws. These glands are among the most complex venomous glands known of all reptiles. In the case of the Komodo dragon, these are compound glands with a larger posterior compartment and five smaller anterior compartments. These compartments have ducts that carry the venom between the teeth.

Even if varanids are closely related to snakes (they share, for example, a bifid tongue), these don’t present the snakes’ characteristic grooves in their teeth. This is due to the fact that instead of injecting the venom directly, monitor lizards use their serrated teeth to open a deep wound in their prey, through which the venom will enter the organism.

Skull of megalania (Varanus priscus) in which we can see the teeth without gooves. This extinct monitor with more than 5 metres long, was the largest venomous animal known. Photo by Steven G. Johnson.

The utility of the venom for the predatory monitors is also supported by the large quantities of venom that they produce. In constrictor snakes that don’t utilise venom, the genes which codify the synthesis of venom are atrophied because of the great amount of energy required to produce it. Monitors, instead, secrete lots of venom with the slightest stimulation of their glands. This venom contains anticoagulant compounds which prevent the wound to close and also produces a cardiovascular shock in the animal by lowering the blood pressure.

A group of Komodo dragons (Varanus komodoensis) feeding on a recently killed pig. Image extracted from Bull, Jessop et al.

Even if we still don’t know for sure if the common ancestor of all these animals was venomous, nor if venom appeared independently in the different families, the relationship between the different members of the clade Toxicofera has been supported by posterior phylogenetic analyses. What we know is that venom is an extremely powerful weapon in the struggle for survival and that, even if snakes are the most numerous venomous reptiles, many other squamate species have been benefiting from the use of toxins, both for self-defence and to subjugate their prey.

REFERENCES

The following sources have been used during the elaboration of this entry:

• Halliday & Adler (2007). La gran enciclopedia de los Anfibios y Reptiles. Editorial Libsa.
• http://www.nature.com/nature/journal/v439/n7076/full/nature04328.html
• http://www.sciencedirect.com/science/article/pii/S0041010114003353
• http://www.leidenuniv.nl/en/researcharchive/index.php3-c=134.htm
• http://www.heloderma.net/en/heloderma.html
• http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0011097
• https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2690028/
• Cover image by Rocío Corzo.

The world from the eyes of a snake

Imagine you are a snake. You’re crawling along the path, with a long slithering body behind you. You have no ears and, even if your eyes are large and well-developed, you cannot blink. You’re constantly flicking your tongue, which informs you about everything that has happened around you, especially about the smell of that tasty mouse you’ve been looking for for days. Ophidians have suffered so many bodily modifications that their senses have had to adapt to their lifestyle. With more than 3,000 current snake species it’s difficult to generalize, but in this entry we’ll explain some of the most curious sensorial adaptations of current ophidians, trying to shed some light over the world of these fascinating and unfairly treated animals.

SMELL: TASTING THE AIR

One of the most developed ophidian senses is smell. It’s common knowledge that snakes use their tongue to smell the air and detect chemical substances. It was once thought that snakes used only their tongue to smell and that the nasal epithelium was only used to activate this mechanism. Now it’s known that snakes smell using both their nose and their tongue, even if the latter is more useful in certain situations.

Microscope image of a transversal slice of a snake skull, where we can see the olfactory epithelium of both the nasal cavity and the vomeronasal organ. Image by Elliott Jacobson.

Snakes taste the air using their tongue and the vomeronasal or Jacobson’s organ. This organ isn’t found only in snakes, as it is also found in other lizards, some salamanders and many mammals. The vomeronasal organ is used to detect non-volatile chemical substances (which need direct contact with the epithelium to be detected) such as pheromones or the scent of a prey.

Scheme of the position of the vomeronasal organ. This forms during the embryonic development from the nasal cavity and it has an opening to the palate. Image by Fred the Oyster.

The snakes’ distinctive bifid tongue is very specialized into particle transport to the vomeronasal organ. It has a set of microscopic papillae or depressions (depending on the species) that help to catch and retain odorous particles. Then it brings this information to the palate, where it gets in contact with the vomeronasal organ.

Monitor lizards (relatives of snakes) also present bifid tongues which allows them to smell the air. Photo of an Asian water monitor (Varanus salvator) from India, by Dibyendu Ash.

Snakes flick their tongue in the air or against some surface to collect “chemical samples” from the environment. Also, the fact that the tongue is bifid is thought to be useful in detecting the direction from where the stimulus comes, as the information obtained from each tip of the tongue goes to one of the two cavities of the vomeronasal organ and goes to the brain by separate ways.

Photo of a European grass snake (Natrix natrix) flicking its tongue to taste the air. Image from WikiImages.

Snakes use this chemical information to follow the trail of a prey, to find a mate and to detect the reproductive state of another individual. Also, a recent study shows that snakes (thanks to their keen sense of smell) are able to recognize their siblings and relatives, choosing them before a stranger to share their hibernation grounds.

Hearing: listening without ears

Hearing is one of the least developed ophidian senses. The absence of an external ear caused that for a long time it was believed that snakes were deaf. Yet recently, it has been demonstrated that snakes do have different methods to detect different types of vibrations.

Portrait of an Indian python (Python molurus) in which the absence of external ears can be seen. Photo by Holger Krisp.

As we explained on an earlier entry, snakes do not have neither external ears nor eardrums. Yet, they do present all the elements of the inner ear characteristic of tetrapods. What changes is the way the vibrational stimulus is transmitted, which in ophidians is accomplished via a bone called columella.

Scheme of the auditory apparatus of a common snake. Image by Dan Dourson.

The columella is a small, long and thin bone attached by ligaments and cartilaginous tissues to the posterior end of the upper jaw and that articulates with the lower jaw. Snakes have one on each side of their skull, which have an equivalent function to the stapes (bones of the mammalian middle ear). The columellas are completely surrounded by tissues, so aerial, terrestrial and aquatic vibrations, are transmitted to these bones which are in contact with the fluids of the inner ear.

Yet, the snakes’ sensitivity to aerial waves is pretty much limited. For example, while human beings are able to hear aerial vibrations between 20 and 20,000 Hz, snakes can only detect vibrations between 50 and 1,000 Hz. Even though they have such limited hearing range, in some species it has been observed that they are able to receive vibrational stimuli with any body part, as these are transmitted through the bodily tissues to the columellas.

Aquatic snakes like the anaconda (Eunectes murinus) can detect with all their body the sounds of an animal moving through the water. Photo by Ddouk.

Even with their limitations to hear aerial waves, what snakes do best is to detect vibrations coming from the ground or the water. Most snakes can detect with great precision vibrations generated by the steps of a prey by keeping their lower jaw (which is in contact with the columellas) in contact with the ground.

The Arabian horned viper (Cerastes gasperettii) is a snake that lives in sand deserts, where the terrain allows a great transmission of terrestrial vibrations. Image by Zuhair Amr.

SIGHT: LIGHT AND HEAT

The eyes of snakes are not very different from the eyes of most terrestrial vertebrates. Yet they have some special characteristics, probably due to their subterranean or subaquatic origins. Most scientists think that snakes had to somehow “reinvent their eyes”.

Some primitive ophidians, like this European blind snake (Typhlops vermicularis), have small and poorly-developed eyes. Image by Kiril Kapustin.

The structure of their eye is mostly identical to that of the rest of tetrapods. A difference is the focusing method: while most tetrapods focus by changing the curvature of the crystalline lens, snakes focus moving the crystalline lens forward and backward. Also, while most terrestrial vertebrates have eyelids to protect the eye, snakes have an ocular scale called the spectacle which is renewed each time they shed their skin.

Western rat snake (Pantherophis obsoletus) about to shed its skin, moment when the spectacle turns opaque. Photo by Bob Warrick.

Depending on the snake’s lifestyle, its sight will have different adaptations, even if in most species the retinas present both rods (sensitive to low light conditions) and cones (allow to see details and colours). Subterranean, more primitive snakes present quite simple eyes, with only rods which allow them to distinguish light and darkness. On the other hand most diurnal snakes have round pupils and both cones and rods.

Many arboreal snakes like this green vine snake (Ahaetulla nasuta) present horizontal pupils which allow them to have a wider range of vision, making it easier to calculate the distance between one branch and another. Photo by Shyamal.

Aside from visible light, some snake are able to see other wavelengths. Pit vipers and some pythonomorphs (pythons and boas) can detect infrared radiation, being able to see the thermic signature around them. This is extremely useful to detect prey in low light conditions, as they can perceive their body heat.

Photos of a python and a pit viper where both the nostrils (black arrows) and the pit organs (red arrows) are highlighted. Image by Serpent nirvana.

They can do this using the pit organs, cavities that appeared independently in pit vipers (from which they got their name) and pythonomorphs. While pit vipers only have a pair of facial pits on both sides of their snout, pythonomorphs have various labial pits on the upper or the lower lip. Despite having fewer pits, the pit vipers’ ones are more sensitive that the ones of the pythons.

Scheme of the structure of a pit organ of a pit viper. This presents a membrane sensible to temperature variations, behind which there’s a chamber with air and nerves sensible to heat. This air dilates when the temperature rises and it activates the trigeminal nerve. Image by Serpent nirvana.

These pits are extremely sensitive and can detect temperature changes of up to 0.001°C. The trigeminal nerve reaches the brain via de optic tectum, making the image detected by the eyes superpose with the infrared image from the pits. Therefore snakes detect both the visible light (as we do) and the infrared radiation in a way that is impossible for us to imagine.

Video from BBCWorldwide in which they explain how a timber rattlesnake (Crotalus horridus) uses infrared detection to hunt a rat in the dark.

As you have seen, snakes perceive the world very differently than we do. Snakes do not leave anyone indifferent and, in the same way that different people see snakes in different ways, different ophidian species present different and diverse adaptations to perceive the world that surrounds them. We hope that with this entry, you’ve been able to understand a little better the incredible world in which snakes live.

REFERENCES

The following sources have been consulted during the elaboration of this entry:

• Harvey B. Lillywhite (2014). How snakes work. Structure, function and behaviour of the world’s snakes. Oxford University Press.
• Halliday & Adler (2007). La gran enciclopedia de los Anfibios y Reptiles. Editorial Libsa.
• Masó & Pijoan (2011). Anfibios y Reptiles de la Península Ibérica, Baleares y Canarias. Ediciones Omega.
• http://news.nationalgeographic.com/news/2004/02/0223_040223_rattlesnakes.htmlutm_content=buffer44d50&utm_medium=social&utm_source=facebook.com&utm_campaign=buffer
• Cover image by Bernard Dupont.

Immaculate Conception… in reptiles and insects

December’s bank holidays and Christmas’s holidays have in common in that the Immaculate Conception is celebrated in both. The biological phenomenon in which a female animal reproduces without mating with a male is called parthenogenesis and, even if there isn’t any proof that this could happen to human beings, virginal birth is a widely distributed thing throughout the animal kingdom. In this entry we’ll see how this incredible phenomenon happens and some species in which it appears.

WHAT IS PARTHENOGENESIS?

Parthenogenesis is a type of asexual reproduction in which the offspring comes from a non-fertilized ovum. Without fertilization (union of the oocyte’s and the sperm’s genetic material) the offspring won’t have any part of the father’s DNA (if there is a father). The resulting babies will be genetic copies (clones) of their mother.

During fertilization, when the ovum and the sperm fuse together (both haploid cells, with just one copy of chromosomes, n chromosomes) a new individual is formed with a unique genetic combination, with DNA from its father and its mother (diploid, with two copies of each chromosome, 2n chromosomes in each cell). Triploid (3n) or tetraploid (4n) individuals only appear in asexual hybrid species, and most cases are non-viable. Images by Ehamberg.

In parthenogenetic animals, the lack of paternal genetic material must be compensated because in many species haploid foetuses are non-viable. In these species diploidy (2n chromosomes) is usually re-established through a process called automixis. Yet in some species, haploid individuals with parthenogenetic origins are viable and have no problems in surviving.

It is impossible to pose a general example for asexual reproduction, as it is widely distributed through very different animal groups and there are many cases with many differences among them. Bellow, we’ll present you some examples of different strategies used by animals to reproduce asexually.

HAPLODIPLOIDY IN BEES AND WASPS

Haplodiploidy is a phenomenon that appears in two insect orders, hymenopterans (bees, ants and wasps) and thysanopterans (thrips or stormbugs). In this sexual determination system, if the ovum is fertilized it will develop into a female while, if it isn’t fertilized a haploid male will be born.

Colony of Carniolan honey bees (Apis mellifera carnica), a subspecies of hony bee from Eastern Europe. Photo by Levi Asay.

In the honey bee, when the queen bee mates with a drone (male bee), all the diploid individuals (2n) will became females, with DNA combined from the queen and the drone. By contrast, drones are born by parthenogenesis, in which an egg from the queen will develop into a haploid drone (n). This means that the individuals in a bee colony, descendants from the same queen, are much more closely related to each other than regular siblings (drones have 100% of their mother’s DNA). It is believed that this helped to the development of eusocial behaviours in different hymenopteran groups.

CYCLIC PARTHENOGENESIS

This kind of parthenogenesis is found in different invertebrate groups that can alternate between asexual and sexual reproduction during its life cycle depending on the environmental conditions.

Diagram about the life cycle of a rotifer, in which parthenogenetic asexual reproduction during good environmental conditions is alternated with sexual reproductions with a haploid male during adverse conditions. Image extracted from Hanson et al. 2013.

Some invertebrate groups like aphids, present asexual parthenogenic reproduction from spring until early autumn, when conditions are favourable. During this stage in many populations we find only females that give birth to more females.

Fast motion video in which we can see how the aphids take advantage during good weather conditions to increase fast and efficiently the number of individuals asexually. Video by Neil Bromhall.

When autumn approaches, parthenogenetic females start giving birth to sexual males and females. Both sexes are born by parthenogenesis and have 100% of their mother’s DNA. Sexual winged individuals then disperse to avoid mating with their own siblings. These will mate and females will lay resistant eggs that will survive winter. In spring these eggs will hatch and give rise to a new generation of parthenogenetic females that will start the cycle again.

TRUE PARTHENOGENESIS IN SQUAMATES

The only vertebrates that show true parthenogenesis are the squamates, with about 50 lizard species and one snake being obligate parthenotes. These are unisexual species, all individuals being females that reproduce asexually without the intervention of any male. Also, there are many other species that, even if they usually reproduce sexually, are also able to reproduce asexually when there are no males available (facultative parthenogenesis).

Desert grassland whiptail lizard (Cnemidophorus uniparens) which, as its scientific name implies, is a parthenogenic species in which all specimens are female. Photo by Ltshears.

There are isolated cases of captive female sharks, snakes and Komodo dragons that have reproduced without fertilization or mating with a male. Yet, this is known as accidental parthenogenesis, because the high mortality of the offspring (surviving between 1/100.000 and 1/million) shows that it is probably due to a failure of the organism, more than an adaptive phenomenon.

Baby Komodo dragon (Varanus komodoensis) born by accidental parthenogenesis at Chester Zoo. Photo by Neil.

Females from the true parthenogenetic species produce haploid eggs (with n chromosomes) which eventually become diploid (2n chromosomes) by two consecutive division cycles during meiosis (automixis). In species with facultative parthenogenesis, diploidy is achieved by the fusion of the ovum with a haploid polar body that forms during meiosis.

Scheme of the formation of polar bodies during oogenesis, which may help parthenogenetic reptiles to regain their diploidy. Scheme by Studentreader.

True parthenogenesis is especially well-known in the Brahminy blind snake (Ramphotyphlops brahminus) and many species of lizards. In these species females generate clones of themselves. Parthenogenetic lizard species (like in amphibians) probably originated from a hybridization event between two sexual species. Many whiptail lizards (genera Cnemidophorus/Aspidoscelis) present unisexual species in which no males exist, from a hybridation process.

Brahminy blind snake (Ramphotyphlops braminus), the only known unisexual ophidian, in which all specimens found to date are females. Photo taken from Kaiser et al. 2011.

The species Cnemidophorus uniparens is a parthenogenic unisexual species, which appeared asa result of the hybridization between C. inornatus and C. burti. The resulting hybrid reproduced again with C. inornatus, forming the triploid (3n) parthenote C. uniparens. The presence of triploid, tetraploid, etc. genomes is a common phenomenon between unisexual reptiles, as its hybrid origins sometimes prevents the mixing of genomes. Also, a greater chromosomal variability compensates the lack of genetic recombination.

Despite being unisexual, sexual behaviours have been observed in this species similar to bisexual species. In C. uniparens there are documented sexual behaviours in which one female takes the role of a male and “mounts” another female contacting their cloacae. It is known that mounted females increase their egg production after this fake copula. It is believed that from one year to the other females shift their roles of mounting or being mounted, varying from year to year the number of eggs laid.

Three species of whiptail lizards. The middle one, Cnemidophorus neomexicanus is an unisexual parthenogenic species, originated from the hybridization of two bisexual species, C. inornatus (left) and C. tigris (right). Photo by Alistair J. Cullum.

Even if they are true parthenogenetic species, many of these squamates keep their ability to add new DNA to their offspring. This is due to the fact that if there’s no genetic recombination by the fusion of the ovum and the spermatozoon, there’s a high risk of accumulating genetic mutations detrimental for the species. Yet parthenogenesis allows these species to quickly colonize new habitats, because it is not necessary for two individuals to find each other to procreate, and 100% of the population is able to reproduce.

As you can see, there is a great number of animals that don’t need males nor sex to reproduce. The existence of a similar process in human beings is pretty much improbable (no to say impossible). Besides, if 2000 years ago a woman would have given birth to a baby without fertilization, probably this would have been a girl, because it wouldn’t have been able to acquire the Y chromosome from anywhere. Yet, this doesn’t mean we cannot enjoy the upcoming holidays. Merry Christmas and Happy New Year to everyone!

REFERENCES

The following sources have been used during the elaboration of this entry:

• Halliday & Adler (2007). La gran enciclopedia de los Anfibios y Reptiles. Editorial Libsa.
• Masó & Pijoan (2011). Anfibios y Reptiles de la Península Ibérica, Baleares y Canarias. Ediciones Omega.
• http://news.nationalgeographic.com/news/2012/09/120914-virgin-birth-parthenogenesis-snakes-science-biology-letters/
• https://www.researchgate.net/publication/280691646_Parthenogenesis_Birth_of_a_New_Lineage_or_Reproductive_Accident
• https://www.researchgate.net/publication/228471514_The_Caucasian_rock_lizard_Lacerta_rostombekovi_a_monoclonal_parthenogenetic_vertebrate
• http://www.ncbi.nlm.nih.gov/pmc/articles/PMC348299/
• http://animals.mom.me/reproductive-cycle-whiptail-lizards-3166.html
• Cover image by Pepper M, Doughty P, Fujita MK, Moritz C, Keogh JS.

Limb regeneration, from the axolotl to human beings

The regeneration of lost or damaged body parts in animals is known from many centuries ago. In 1740 the naturalist Abraham Trembley observed a small cnidarian that could regenerate its head if it was cut off, so he called it Hydra, in reference to the monster from Greek mythology that could grow back its multiple heads if they were cut off. Afterwards, it was discovered that there were many other species of animals with regenerative abilities. In this entry we’ll talk about these animals.

Regeneration in the animal kingdom

Regeneration of body parts is more widespread between the different groups of invertebrates than it is between the vertebrates. This process can be bidirectional, in which both parts of the animal regenerate their missing parts to form two animals (just like the hydra, planarians, earthworms and starfishes) or unidirectional, in which the animal loses an extremity but it just regenerates, without forming two animals (arthropods, molluscs and vertebrates). In vertebrates, fishes and amphibians are the ones that present the greatest regenerative capacities, although many lizards and some mammals are able to regrow their tails.

Image by Matthew McClements about bidirectional regeneration in planarians, hydras and seastars. Extracted from Wolbert's Principles of Development.

Regeneration can be done by two different ways:

• Regeneration without active cellular proliferation or “morphallaxis”. In this type, the absent body part is regrown through remodelling of pre-existing cells. This is what happens in the Hydra, in which lost body parts are regenerated without the creation of new material. So, if a hydra is cut in half, we’ll obtain two smaller versions of the original hydra.

Video about an experiment in which an Hydra has been cut in different pieces. Video by Apnea.

• Regeneration with cellular proliferation or “epimorphosis”. In this type, the lost part is regenerated via cellular proliferation, it is “newly created”. In most cases, it happens through the formation of a specialized structure called blastema, a mass of undifferentiated cells which appears during phenomena of cellular regeneration.

Almost all groups of animals with regenerative capacities present regeneration with blastema formation. Yet the origin of the blastemal stem cells varies between groups. While planarians present pluripotent (that can differentiate to any kind of cell type) stem cells all along their bodies, vertebrates have specific cells in each type of tissue (cartilage, muscle, skin…) that only regenerate cells of the tissue they come from.

In land vertebrates, lizards and urodeles are the ones that present the most powerful regenerative abilities. Down below we’ll see how they regenerate and the applications it has in modern human medicine.

Expendable tails

When you are a small animal that is being chased by a cat or any other predator, it probably is better for you to lose your precious tail than to lose your life. Some terrestrial vertebrates have evolved following this philosophy, and they are able to shed off their tails voluntarily through a process called caudal autotomy. This allows them to escape from their predators, which are entertained with the still moving lost tail.

 Video in which we can see how some lizards like this red-tailed vanzosaur (Vanzosaura rubricauda) have brightly coloured tails to attract the attention of predators. Video by Jonnytropics.

Autotomy or self-amputation, is defined as a behaviour in which the animal can shed off one or more body parts. Caudal autotomy is found in many species of reptiles and in two species of spiny mouse of the genus Acomys. In reptiles we can find caudal autotomy in lacertids, geckos, skinks and tuataras.

Foto of a Cairo spiny mouse (Acomys cahirinus), a mammal which is able to shed and regrow its tail. Photo by Olaf Leillinger.

In reptiles, the fracture of the tail happens in specific areas of the caudal vertebras which are naturally weakened. The autotomy may happen in two different ways: intravertebral autotomy, in which the vertebra at the centre of the tail have transversal fracture planes prepared to break if they are pressed hard enough, and intervertebral autotomy, where the tail breaks between vertebras by muscular constriction.

Tridimensional model of the fracture planes on the tail of a lizard and the regeneration post-autotomy of a cartilaginous tube. Image extracted from Joana D. C. G. de Amorim et al.

Caudal autotomy allows the animal to escape, but it isn’t without cost. Many reptiles use their tails as a reserve of fat and losing this energy store is usually detrimental for the animal. That’s why many lizards, once the threat has disappeared, look for their lost tail and eat it, to at least regain the energy it had as fat. In addition, regenerating a new tail requires a great expenditure of energy.

Photo of a Catalonian wall lizard (Podarcis liolepis) that has shed its tail. Photo by David López Bosch.

The regeneration of the tail in reptiles differs from that of amphibians and fishes in that it happens without the formation of a blastema and instead of an actual regeneration of the caudal vertebras, it forms a cartilaginous tube along it. The new tail is stiffer and shorter than the original one, and it usually regenerates whole some weeks after the amputation. Most lizards can regenerate their tails multiple times, but some species like the slow worm (Anguis fragilis) can only do it once. Sometimes, the original tail isn’t completely broken but the regeneration mechanisms are activated, which can lead to lizards and geckos with more than one tail.

Detail of the tail of a common wall gecko (Tarentola mauritanica) which has regenerated the tail without losing its original tail. Photo by Rafael Rodríguez.

Urodeles, the kings of regeneration

Of all tetrapods, amphibians are the ones that present the more astonishing regenerative capacities. During the larval stage of most species, both the tail and the limbs (if they have them) can be regenerated after its loss. The scientific community thinks that this is due to the fact that in amphibians the development of limbs and other organs is delayed until the moment of metamorphosis. Yet, frogs and toads (anurans) only maintain their regenerative powers during their tadpole stage, losing them when reaching adulthood.

Wood frog tadpole (Rana sylvatica) which, like all amphibians, delays the development of its legs up to the moment of metamorphosis. Photo by Brian Gratwicke.

Instead, many salamanders and newts (urodeles) conserve their regenerative powers their whole life. Even if many species present caudal autotomy, unlike lizards urodeles are able to completely regenerate, not only their tails, but practically any kind of lost body tissue. Of all known species, the axolotl (Ambystoma mexicanum), a neotenic amphibian which reaches adulthood without undergoing metamorphosis, has served as a model organism for the study of the formation of the blastema that precedes regeneration.

 Video about the axolotl, this curious amphibian which is greatly endangered. Video by Zoomin.TV Animals.

Regeneration as it happens in salamanders has stages genetically similar to the ones that occur during the development of the different body tissues and organs during the embryonic development of the rest of vertebrates. In the axolotl (and in the rest of urodeles) regeneration of a limb after amputation goes through three different stages:

• Wound healing: During the first hour after the amputation, epidermal cells migrate to the wound. The closing of the wound usually completes two hours later with the same mechanisms as in the rest of vertebrates. Yet, the complete regeneration of the skin is delayed up until the end of the regeneration.
• Dedifferentiation: This second phase, in which the blastema is formed, starts 24 hours after amputation. This is composed both of cells from the specialized tissues of the amputated zone which lose their characteristics (they obtain the capacity to proliferate and differentiate again) and cells derived from the connective tissue that migrate to the amputation zone. When these cells of different origins accumulate and form the blastema, the cellular proliferation starts.
• Remodelling: For the third stage to start, the formation of the blastema is required. Once the blastema is formed by different dedifferentiated cells, the formation of the new limb follows the same pattern as any kind of vertebrate follows during embryonic development (it even has de same genes intervening).

Diagram about the formation of the blastema in a zebrafish (Danio rerio) another model organism. Image from Kyle A. Gurley i Alejandro Sánchez Alvarado.

Recently fossils have been found from many different groups of primitive tetrapods which present signs of regeneration. Proof has also been found of limb regeneration in temnospondyl (Apateon, Micromelerpeton and Sclerocephalus) and lepospondyl (Microbrachis and Hyloplesion) fossils. This wide variety of basal tetrapod genera presenting regeneration and the fact that many fish also present it, has led many scientists to consider if the different groups of primitive tetrapods had the ability to regenerate, and if it was lost in the ancestors of amniotes (reptiles, birds and mammals).

Photo of an axolotl, by LoKiLeCh.

However, it is believed that the genetic information that forms the blastema could still be found in the DNA of amniotes but in a latent state. Of the three stages of the regeneration process, the only one exclusive to urodeles is the dedifferentiation stage, as the healing stage is the same as in the rest of vertebrates and the remodelling stage is like the one during embryogenesis. Currently many studies are being carried out on the way to reactivate the latent genes that promote the formation of the blastema in other vertebrates, such as humans.

Some human organs like the kidneys and the liver already have some degree of regenerative capacities, but thanks to investigation with stem cells in animals like salamanders and lizards currently it is able to regenerate fingers, toes, genitals and parts of the bladder, the heart and the lungs. As we have seen, the different animals able to regenerate amputated limbs hold the secret that could save thousands of people. Remember this the next time you hear that hundreds of species of amphibians and reptiles are endangered because of human beings.

References

During the writing of this entry the following sources have been consulted:

• Cover photo by Peter Halasz.
• Halliday & Adler (2007). La gran enciclopedia de los Anfibios y Reptiles. Editorial Libsa.
• http://www.eurostemcell.org/de/node/19896
• https://www.ncbi.nlm.nih.gov/pubmed/12455626
• https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3480082/
• http://ftp.eebweb.arizona.edu/courses/Ecol483_583/Bateman%20and%20Fleming%202009.pdf
• http://www.sciencemag.org/content/276/5309/81.short
• http://www.ambystoma.org/
• http://www.nature.com/nature/journal/v527/n7577/full/nature15397.html

Herpetological parachuting: gliding amphibians and reptiles

Currently, the only flying reptiles are birds, direct descendants of theropod dinosaurs. Although the age of the great flying reptiles has passed, nowadays, various species of reptiles and amphibians have acquired the ability of gliding to escape their predators. Gliding is defined as falling at an angle less than 45^o from the horizontal with the help of membranes that create resistance to the air. In this entry I’ll show you some gliding herp species which currently exist.

Gliding frogs

Gliding frogs (also called “flying frogs”) include species from the Polypedates, Rhacophorus (Rhacophoridae family) and Ecnomiohyla (Hylidae family) genera. These have gained similar characteristics through a process of convergent evolution.

Photo of Ecnomiohyla rabborum by Brian Gratwicke.

Both hylids and rhacophorids are popularly known as tree frogs. Their limbs are specialized for an arboreal lifestyle, with long legs and fingers with sucker-like structures for a better grip.

 Male and female false Malabar's gliding frogs (Rhacophorus pseudomalabaricus) mating. Video by Sandesh Kadur.

The gliding genera have also acquired big membranes on its limbs and between their toes to help them glide and therefore, being able to escape predators more efficiently.

Wallace's flying frog (Rhacophorus nigropalmatus) gliding.

Gliding geckoes

Between the members of the Gekkonidae family there are two Southeast Asian genera which have acquired adaptations for gliding: the Ptychozoon genus and the Luperosaurus genus.

Photo of a Kuhl's flying gecko (Ptychozoon kuhli) by Bernard Dupont.

Geckoes are a group of lizards which have evolved for an arboreal lifestyle which allows them to adhere practically on any surface. Their feet present tiny filaments which allow them to move even upside down.

Detail of the underside of a Kuhl's flying gecko (Ptychozoon kuhli) in which the skin flaps can be appreciated. Photo by Fenchurch.

The Ptychozoon and Luperosaurus genera also present membranes on their neck, body, limbs and tail that help them to blend in the surface of trees and also to glide at some extent from tree to tree to escape possible predators.

Flying snakes

Speaking of predators, the snakes from the Chrysopelea genus also have developed an efficient method to move through the rainforest’s canopy. The snakes from this genus are diurnal, feed on lizards, frogs, birds and bats, and are found throughout Southeast Asia.

Couple of Paradise flying snakes (Chrysopelea paradisi) in the Singapore Zoo, by Alan Couch.

Unlike the former gliding herps, flying snakes have no membranes to slow down their descent, instead they have a more complex method. When arriving at the tip of a tree branch, these snakes drop themselves. After a brief fall, they retract their inner organs, compressing them against their thoracic cavity and flaring out their ribs laterally, taking a semi-concave shape, similar to that of a plane’s wing.

Explicative image of the gliding mechanism of the flying snakes. Image from Biomechanics.

With this method and with the help of serpentine movements, the snakes of the Chrysopelea genus can control with great precision the direction of their descent. These snakes have a more controlled glide than many gliding mammals such as the gliding squirrel and are able to glide through a horizontal length of up to 100 metres.

 Group of scientists testing a Paradise flying snake’s (Chrysopelea paradisi) ability to glide. Video by All of These Videos.

Flying dragons

And we finally get to the most spectacular of all flying herps, the reptiles known as flying dragons. These agamids (Agamidae family) of the Draco genus are found in the tropical forests of Asia, where they survive hunting insects on the forest canopy.

Photo of a five-lined flying dragon (Draco quinquefasciatus) from Sarawak, Malaysia. Image by Bernard Dupont.

The main characteristic of flying dragons is their ribs, some of which are extremely elongated and present dermal membranes between them acquiring the function of wings. These “wings” are usually retracted against the body and can be erected for both gliding and sending visual signals to other members of their species (wings are usually brightly coloured).

Drawing from the book On The Genesis of Species of the skeleton of a Draco volans.

Flying dragons use their wings to move from tree to tree, to hunt, to escape predators, to chase their own kind during both territorial disputes and courtship. Aside from their brightly coloured wings, many species also present colourful dewlaps (especially males) to indicate their reproductive state to other members of their species.

Photo of a Sulawesi's lined flying dragon (Draco spilonotus) by A. S. Kono.

The flight record of these agamids is of 60 metres of distance with a vertical descent of only 10 metres. Flying dragons are small, fast and active animals, so few predators are able to hunt them. In addition, they are totally arboreal with only females descending to the ground to lay their eggs underground.

 Flying snake chasing a flying dragon. Video found in Venomous Animals.

As we have seen, most species of gliding amphibians and reptiles live in tropical climates. This is due to the fact that these are habitats with a dense vegetation cover and trees grow very close to one another, allowing these animals to glide from one tree to the other easily. The main threats to these creatures are deforestation and habitat loss since, without an optimal vegetation cover, these animals may be preyed easily by terrestrial predators.

References

During the elaboration of this entry the following sources have been used:

• Cover photo: Premaphotos.
• Halliday & Adler (2007). La gran enciclopedia de los Anfibios y Reptiles. Editorial Libsa.
• http://australianmuseum.net.au/blogpost/science/aerodynamic-amphibians
• http://www.naturia.per.sg/buloh/verts/flying_tree_snake.htm
• http://www.siam-info.com/english/snakes_chrysopelea.html
• http://phys.org/news/2005-05-reveal-secrets-snake-flight.html
• http://www.uchospitals.edu/news/2005/20050513-snake.html

How do temperature and global warming affect the sex of reptiles?

In most animals the sex of an individual is determined at the moment of fertilization; when the egg and the sperm fuse together it is fixed if that animal will be male or female. Yet in many reptilian groups sex determination is established later during incubation, and the determinant external factor is the incubation temperature of the eggs. In reptiles, this means that the environment plays a crucial role in determining the sex ratio emerging from an egg clutch, and that these animals are very susceptible to alterations in temperature caused, for example, by climate change.

SEXUAL DETERMINATION: GSD VS TSD

In the majority of animal species, sexual differentiation (the development of ovaries or testes) is determined genetically (GSD). In these cases, the sex of an individual is determined by a specific chromosome, gene or allele which will cause the differentiation to one sex or the other. In vertebrates there exists two main types of GSD, the XX/XY system in mammals (in which XX is a female and XY is a male) and the ZW/ZZ system in birds and some fishes (ZW corresponds to a female and ZZ to a male).

Examples of different types of genetic sexual determination systems found in vertebrates and invertebrates, by CFCF.

In the case of reptiles, there is a great variety of sexual determination mechanisms. Some present GSD models; many snakes follow the ZW/ZZ system and some lizards the XX/XY. Still, in many groups the sex of the offspring is determined mainly by the egg incubation temperature (TSD), and therefore the environment plays an important role in the proportion of males and females found in a population.

The eastern bearded dragon (Pogona barbata) is an example of a reptile with GSD, but which is also affected by incubation temperature. Photo by Trent Townsend.

Nevertheless, the genetic and temperature sexual determination are not mutually exclusive. Reptiles with TSD have a genetic base for the ovarian and testicular differentiation which is regulated by temperature. Similarly, it’s been observed that in reptiles with DSG, such as the eastern bearded dragon (Pogona barbata), high temperatures during incubation causes genetically male individuals (ZZ chromosomes) to develop functionally as females. This proves that in reptiles, there is no strict division between GSD and TSD.

TEMPERATURE AND SEX

The incubation period during which the sex of an individual is determined is called thermosensitive period and usually corresponds to the second third of the incubation period, during which temperature must be maintained constant. This critical incubation period usually lasts between 7 and 15 days, depending on the species. After this period the sex of an individual usually cannot be reversed (all or nothing mechanism).

Komodo dragon baby (Varanus komodoensis) hatching. Photo by Frank Peters.

Temperature during the critical incubation period affects the functioning of the aromatase, a hormone which converts androgens (masculinizing hormones) to estrogens (feminizing hormones). At male-producing temperatures, the activity of the aromatase is inhibited, while at female-producing temperatures the activity of the aromatase is maintained.

Graphics of the aromatase’s activity related to gonadal hormones on European pond turtle’s embryos (Emys orbicularis) at 25oC (males) and at 30oC (females), during the critical incubation period, from Pieau et al. 1999.

The TSD is found in all reptile groups except snakes (which have the ZW/ZZ system). In lizards and turtles we can find both genetic-based and temperature-based sexual determination, while in tuataras and crocodilians sex is determined exclusively by temperature. Currently, different patterns of temperature sex determination are known.

PATTERN I

This pattern is the simplest one, in which higher incubation temperatures produce one sex and lower incubation temperatures produce the other sex. Intermediate temperatures usually produce individuals of both sexes and very rarely, intersex individuals. This pattern can be further divided in:

• Pattern Ia TSD, in which eggs incubated at warmer temperatures produce high female percentages and eggs incubated at cooler temperatures produce high male percentages. This pattern is found in many species of turtles.

Photo of a European pond turtle (Emys orbicularis), species that follows the pattern Ia TSD; at 25oC or less during incubation only males are born, while at 30oC or more only females are born. Photo by Francesco Canu.

• Pattern Ib TSD, in which the contrary occurs; high temperatures produce males and low temperatures produce females. We find this pattern in some lizards with TSD and in the tuataras.

The tuatara (Sphenodon punctatus) is one of the reptiles that follows the pattern Ib TSD; the pivotal temperature is between 21-22oC, above which males will be born and below which females will be born.

PATTERN II

This pattern is a bit more complex than the previous one. In this one, embryos incubated at extreme temperatures (very high or very low) will differentiate to one sex, while the ones incubated at intermediate temperatures will differentiate to the other sex.

Photo of different aged American alligators (Alligator mississippiensis). These reptiles follow the pattern II TSD; at about 34oC males are born, and at higher and lower temperatures, females are born.

This pattern appears in crocodilians, some turtles and in many lizards. Recent phylogenetic studies indicate that this is the ancestral TSD model in reptiles. Some people even argue that all the TSD cases belong to the pattern II, but that in nature temperatures never reach both extremes, although this is yet to be proved.

TEMPERATURE DETERMINED SEX: PROS AND CONS

Even today the evolutionary advantages of the sex determination by temperature are not fully understood. The case of the reptiles is pretty curious because birds, mammals and amphibians determine their sex genetically in most cases, while in reptiles there is a bit of everything.

Currently, there are studies which are being conducted to see if certain temperatures improve the health of males and if other temperatures the health of females. In one of these studies, it was observed that snapping turtles incubated at intermediate temperatures (which produced both males and females) were more active than the ones incubated at temperatures producing only one sex, making them more vulnerable to be attacked by sight-based predators. Currently, there isn’t enough evidence that indicates to what extent these discoveries could be applied. It is possible that reptiles with TSD are able to manipulate the sex of its offspring, altering the proportion of sexual hormones based on the temperature of their nesting site.

Common snapping turtle (Chelydra serpentina) an American fresh-water chelonian, laying its eggs. Photo by Moondigger.

The disadvantages of the TSD are much easier to predict.  Any change in the environmental temperature of the nesting areas may affect negatively the populations of a determined species. If a previously shadowy forest is cut down or buildings are constructed in a previously sunny place, the microclimates of the egg clutches of any reptile nesting there will be changed.

Global change, or climate change, represents an additional threat to reptilians with TSD. The rise of the average temperature on the planet and the temperature fluctuation from one year to another, affect the number of males and females that are born in some species of reptiles. This phenomenon has been observed, for example, in painted turtles (Chrysemys picta), in which it has been predicted that a rise of 4^oC in their habitat’s temperature could cause the extinction of the species, because only females would be born.

Baby of a painted turtle (Chrysemys picta), species in which incubation temperatures between 23-27oC produce males, and temperatures above and below it produce females (pattern II). Foto de Cava Zachary.

REFERENCES

During the elaboration of this entry the following sources have been used:

• Cover photo: Animalspot.
• Halliday & Adler (2007). La gran enciclopedia de los Anfibios y Reptiles. Editorial Libsa.
• http://www.scientificamerican.com/article/experts-temperature-sex-determination-reptiles/
• http://www.ncbi.nlm.nih.gov/books/NBK9989/
• http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2603247/
• https://embryo.asu.edu/pages/temperature-dependent-sex-determination-reptiles
• http://onlinelibrary.wiley.com/doi/10.1002/jez.465/abstract
• http://link.springer.com/article/10.1007/s000180050342#page-2
• http://www.nbcnews.com/science/weird-science/hotter-temperatures-trigger-sex-change-australian-lizards-n385241
• http://www.herpconbio.org/Volume_5/Issue_2/Nelson_etal_2010.pdf