Amphibians

The Plethodontidae is by far the largest family of salamanders, comprising nearly 70% of all living species. In total there are 378 known plethodontids divided between four subfamilies and 24 genera. The plethodontids are united by the fact that they do not possess lungs and breathe entirely through their skin and mouth lining. They are often referred to as the lungless salamanders, although they are thought to have evolved from highly aquatic, lunged ancestors in the streams of the Appalachian Mountains in eastern North America. The earliest plethodontids were hypothesised to have lost their lungs because individuals with reduced, or absent, lungs were less likely to float away in the swift mountain streams where they lived. The vast majority of other salamanders possess lungs, so this makes the lungless salamanders an unusual and fascinating group of animals.

They are thought to have diverged from all other amphibian species 145 million years ago at the boundary between the Jurassic and Cretaceous periods. They are as different from all other amphibian lineages as wombats are from whales, evolving at a time when dinosaurs were still dominant. Overall, plethodontids are the most evolutionary advanced salamanders, so it may at first appear odd that they should have lost lungs, which are one of the most basic features of all vertebrates living on land. Lacking lungs and being dependent on their skin for respiration places a size restriction on these salamanders because large animals have a relatively small surface area of skin compared to their body’s volume, and have greater difficulty in supplying their body tissues with oxygen compared to smaller animals (which have a large surface area to volume ratio). The long, slender form of the lungless salamanders maximises the surface area available for gas exchange, and some species grow to lengths of over 300 mm.

Plethodontid salamanders occupy a great diversity of habitats, ranging from strictly aquatic to strictly terrestrial, exploring niches as diverse as caves, trees, mountain streams, and they are also found burrowing through the earth. Dependence on their skin for breathing places limitations on where and how lungless salamanders can live. Their skin must be kept moist at all times in order for oxygen to be taken up by the blood in capillaries beneath the skin. This means plethodontids are either confined to humid areas, or must find damp hiding places and only emerge in wet weather, typically at night. The life of a lungless salamander in less humid areas, like Europe and temperate North America, therefore comprises brief periods of activity interspersed with inactive phases that are often very long. They are able to survive the periods of inactivity because they have a very low metabolic rate and low energy requirements. Able to store much of what they eat as fat, they do no need to feed very often.

A further adaptation, present among many species of the lungless salamander subfamilies named “Plethodontinae” (from East and West North America) and “Bolitoglossinae” (from tropical Central and South America), is “direct development”. This is a method of amphibian development where the larval stage (e.g. the tadpole stage in a frog’s life history) has been eliminated. Early development takes place in eggs, which may be laid in moist places away from water, and the young hatch out as miniature adults. The well known amphibian metamorphosis, most commonly appreciated in the transition from tadpole to adult frog, does not occur outside of the egg. This mean that certain lungless salamanders in these two subfamilies may live away from water bodies, allowing them to expand their ranges to new areas.

The history and characteristics of the lungless salamanders go some way to explaining their range. They are mostly found in the New World, where they are widely distributed in eastern and western North America, as well as Central and South America. However, continental drift over millions of years has also brought them to the Old World, where they are found in parts Europe (e.g. Sardinia) and Korea. The existence of the Korean crevice salamander was unknown until 2005, when its discovery was a shock to science, indicating a long history of lungless salamanders in Asia. This is the only known species is Asia, suggesting that the rate of species generation in this part of the world is very low, especially compared the the huge radiation of lungless salamander species in the New World.

There are 23 known species in the genus Thorius (commonly known as the “Mexican pigmy salamanders”) which represent one of ten genera present within a lungless salamander subfamily called the “Bolitoglossinae”, including all the plethodontids from Central and South America. The Mexican pigmy salamanders include the smallest salamanders on earth – the most diminutive of which measure just 26.9 mm in total length as sexually mature adults. Thorius salamanders occur only in Mexico, where they are restricted to the southern states of Veracruz, Puebla, Oaxaca and Guerrero. In general, Mexican pygmy salamanders live at high elevations, ranging from about 1,500-3,000 metres above sea level or higher, but some species descend to 800 metres above sea level.

Most Mexican pigmy salamanders lack teeth and their skulls are extraordinary because of the poor state of development, the thinness of the bones, and the weak articulation of the elements. Miniaturisation has been achieved by the reduction or loss of some of the cranial (or skull) elements, accompanied by a relative increase in the size of the sense organs. Another interesting feature of these salamanders is that they possess male heterogamy reproduction – the presence of an X or Y-type sex chromosomes in the eggs and sperm, as is the case in humans. This is known as chromosomal sex determination, where females have two X sex chromosomes (XX) in their cells and males have one X chromosome and one “male” Y chromosomes (XY). In non-chromosomal sex determination, being male or female can occur as a result of environmental conditions, such as temperature, whereas with the X and Y-chromosome system, sex is determined from the outset.

The genus Thorius is thought to have originated in the Early to Mid Miocene period, between 23 and ~12 million years ago. This makes Mexican pigmy salamanders as dissimilar to their closest relative as humans are to gibbons. Specifically, within the Thorius salamanders the Veracruz pigmy salamander diverged about 5 million years ago, and is closely related to another top 100 EDGE species: the San Martìn Pigmy salamander (Thorius narismagnus).

The Veracruz pigmy salamander, like all lungless salamanders in the Bolitoglossinae subfamily, possesses a slender body, long tail and prominent eyes. A distinctive feature of the plethodontid family is a narrow groove (the nasolabial groove) running from each nostril to the upper lip: its function is to carry waterborne odours from the ground into the nasal cavity. Another curious trait of the lungless salamanders are mental (from the Latin “mentum”, meaning chin) glands. These are modified mucus glands and release pheromones, which are chemicals produced by an animal to influence the behaviour of other members if its species, often with regard to breeding receptivity. Mental glands are sometimes visible in males as raised bumps below their lower lip.

Lungless salamanders are very small to medium in size, usually measuring between 25 to 250 mm from the tip of the nose to the end of the tail, which salamanders retain throughout their life. They are unusual among the salamanders in that some species can detach from their tail as a predator-defence mechanism (also known as tail or caudal autotomy). It is therefore not unusual to see individuls missing part or all of their tail, which they may regererate later. Lungless salamanders may have bold patterns on their skin as adults, or they may have a colouration more similar to their environment to aid camouflage. They have well-developed “costal” grooves (successive vertical grooves in the skin along the sides of the body), generally numbering between 12-15. Their limbs are slender and often have largely or completely webbed digits. Species, like the Veracruz pigmy salamander, in the Thorius genus (the “Mexican pigmy salamander”) are very similar in form to those in the genus Bolitoglossa (the “mushroom-tongue salamanders”), although they are generally much small, the largest representatives seldom exceeding 70 mm in total length.

The Veracruz pigmy salamander is a small species, growing to a total length of 49 mm, 23 mm of this measurement being accounted for by the stout tail. The head is slightly wider than the neck and the snout projects slightly beyond the mouth. There are 13 “costal” grooves along either side of the body. This species has slender, weak limbs with very small digits. The skin is smooth, and yellowish brown in colour along the dorsal (or upper) surface. A grey band extends along the back to the tip of the tail. This band is particularly light and slightly metallic along its undulating or serrated margins, and is marked by a number of short V-shaped spots which appear in pairs, one to each costal band (the body segments bordered by the costal grooves). The colouration of the ventral surface (or underside) is brown.

This species is known only from central western Veracruz, from Soledad Atzompa in the south and west, east to Cerro Chicahuaxtla, north to Teocel, Mexico, generally at altitudes of 1,000-1,200 metres above sea level (although it has been found as high as 2,000 metres).