Temporal range: Cambrian - Recent
|Global range of Onychophora: Peripatidae in green, Peripatopsidae in blue|
The velvet worms (Onychophora - literally "claw bearers") form a branch of the group Ecdysozoa and can be simply described as "worms with legs". Most common in the Southern Hemisphere, they prey on smaller animals such as insects, which they catch by squirting a sticky slime. In modern zoology they are particularly renowned for their curious mating behaviour and the fact that they bear live young. The Lobopoda, possible ancestors of velvet worms from the Cambrian period, are of great interest in paleontology.
Velvet worms are very probably close relatives of the Arthropoda and Tardigrada, with which they form the taxon Panarthropoda. The first type was scientifically described in 1825 by Lansdown Guilding, who regarded them to be modified snails (Gastropods); the name Onychophora was not coined until 1853.
- 1 Structure
- 2 Distribution and habitat
- 3 Locomotion
- 4 Diet
- 5 Predators and parasites
- 6 Reproduction and lifecycle
- 7 Conservation status
- 8 Phylogeny
- 9 Taxonomy
- 10 References
Velvet worms are worm-like, segmented creatures with a flattened cylindrical body cross-section and rows of unstructured body appendages known as stub feet. The animals grow to between 0.5 and 20 cm, with the average being about 5 cm, and have between 13 and 43 pairs of legs. Their skin consists of numerous, fine transverse rings and is often inconspicuously coloured orange, red or brown, but sometimes also bright green, blue, gold or white and occasionally patterned with other colours.
Segmenting - outwardly inconspicuous and identifiable only in the regular spacing of the pairs of legs - is shown in the regular arrangement of skin pores, excretion organs and concentrations of nerve cells. The individual body sections are largely unspecialised; even the head develops only a little differently from any abdomen segment. Segmentation is apparently specified by the same gene as traceable in other groups of animals, and is activated in each case, during embryonic development, at the rear border of each segment and in the growth zone of the stub feet.
The "stub feet" which characterise the velvet worms are conical, baggy appendages of the body, which are internally hollow and exhibit no joints. Although the number of feet can vary considerably between species, their structure is basically very similar. Rigidity is provided by the hydrostatic pressure of their fluid contents, and movement is usually obtained passively by stretching and contraction of the animal's entire body. However, each leg can also be shortened and bent by internal muscles; due to the lack of joints, this bending can take place at any point along the sides of the leg.
In some species, two different organs are found within the feet:
- Crural glands are situated at the 'shoulder' of the legs, extending into the body cavity. They open outwards at the crural papillae - small wartlike bumps on the belly side of the leg - and secrete chemical messenger materials called pheromones. Their name comes from the Latin cruralis meaning "of the legs".
- Coxal vesicles are pouches located on the belly side of the leg which can be everted and probably serve in water absorption. They are only found within the family Peripatidae and are named from coxa, the Latin word for "hip".
On each foot is a pair of retractable, hardened (sclerotised) chitin claws, which give the taxon its scientific name: Onychophora is derived from the Greek onyches: "claws"; and pherein: "to carry". At the base of the claws are three to six spiny 'cushions', on which the leg sits in its resting position and on which the animal walks over smooth substrates; the claws are used mainly to gain a firm foothold on uneven terrain.
Apart from the pairs of legs there are three further body appendages, which are at the head and comprise three segments:
- On the first head segment is a pair of slender antennae, which serve in sensory perception. They probably do not correspond directly to the antennae of the Arthropoda, but perhaps rather with their "lips" or labrum. At their base is found a pair of simple eyes, except in a few blind species. In front of these, in many Australian species, are various dimples the function of which is not yet clear. It appears that in at least some species, these serve in the transfer of sperm cell packages (spermatophores).
- On the belly side of the second head segment is the labrum, a mouth opening surrounded by sensitive "lips". In the velvet worms this structure is a muscular outgrowth of the throat, so despite its name it is probably not homologous to the labrum of the Arthropoda. Deep within the oral cavity lie the sharp, crescent-shaped "jaws" or mandibles, which are strongly hardened and resemble the claws of the feet, with which they are probably homologous. The jaws are divided into internal and external mandibles and are covered with fine toothlets. They move backward and forward in a longitudinal direction, tearing apart the prey.
- On the third head segment, to the left and right of the mouth, are two openings designated "oral papillae". Within these are a pair of large, heavily internally-branched slime glands. These lie roughly in the centre of the body and secrete a sort of milky-white slime which is used to ensnare prey and for defensive purposes. Sometimes the connecting "slime conductor" is broadened into a reservoir, which can buffer pre-produced slime. The slime glands themselves are probably modified crural glands.
All three structures correspond to an evolutionary origin in the leg pairs of the other segments.
Skin and musculature
Unlike the arthropods, velvet worms do not possess a rigid exoskeleton. Instead, their body shape is maintained - like a water-filled balloon - by the easily-increased pressure of the internal liquid on the body wall. Because this liquid is incompressible (its volume does not change), muscles can perform work against it. Because the "skeleton material" is effectively water, one can consider the velvet worm to have a "hydraulic skeleton".
The body wall consists of a non-cellular outer skin, the cuticula; a single-layer of epidermis cells forming an internal skin, and beneath this usually three layers of muscle which are embedded in connective tissues.
The cuticula is about a micrometer thick and covered with fine villi. In composition and structure it resembles the cuticula of the arthropods, consisting of α-chitin and various proteins, although not containing collagen. It can be divided into an external epicuticula and an internal procuticula, which themselves consist of exo- and endo-cuticula. This multi-level structure is responsible for the high flexibility of the outer skin which enables the velvet worm to squeeze itself into the narrowest crevices. Although outwardly water-repellant, the cuticula is not able to prevent water loss by respiration and as a result velvet worms can only live in microclimates with high humidity to avoid desiccation.
The surface of the cuticula is scattered with numerous fine papillae, the larger of which carry visible villi-like sensitive bristles. The papillae themselves are covered with tiny scales, lending the skin a velvety appearance. It also feels like dry velvet to the touch, for which its water-repellant nature is responsible. Moulting of the skin (ecdysis) takes place regularly, sometimes every 14 days, induced by the hormone ecdyson.
At each moult, the shed skin is replaced by the epidermis which lies immediately beneath it; unlike the cuticula, this consists of living cells. Beneath this lies a thick layer of connective tissue, which is composed primarily of collagen fibres aligned either parallel or perpendicular to the body's longitudinal axis. Within the connective tissue lie three continuous layers of unspecialised smooth muscular tissue. The relatively thick outer layer is composed of annular (sphincter) muscles and the similarly voluminous inner layer, of longitudinal muscles. Between them lie thin diagonal muscles which wind backward and forward along the body axis in a spiral. Between the annular and diagonal muscles exist fine blood vessels, which lie below the superficially-recognisable transverse rings of the skin and are responsible for the pseudo-segmented markings.
Beneath the internal muscle layer lies the body cavity. In cross-section, this is divided into three regions by so-called dorso-ventral muscles, which run from the middle of the underbelly through to the edges of the upper side: a central mid-section and on the left and right, two side regions which also include the legs.
Haemocoel and circulation
The body cavity is known as a "pseudocoel" or "haemocoel". Unlike a true coelom, a pseudocoel is not fully enclosed by a cell layer derived from the embryonic mesoderm. A coelom is however formed around the gonads and the waste-eliminating nephridia.
As the name 'haemocoel' suggests, the body cavity is filled with a blood-like liquid, in which all the organs are embedded; in this way they can be easily supplied with nutrients circulating in the blood. This liquid is colourless as it does not contain pigments; for this reason it only serves a limited role in oxygen transport. Two different types of blood cells (or haemozytes) circulate in the fluid: amoebocytes and nephrocytes. The amoebocytes probably function in protection from bacteria and other foreign bodies; in some species they also play a role in reproduction. Nephrocytes absorb toxins or convert them into a form suitable for elimination by the nephridia.
The haemocoel is divided by a horizontal partition, the diaphragm, into two parts: the pericardial sinus along the back, and the perivisceral sinus along the belly. The former encloses the tube-like heart and the latter, the other organs. The diaphragm is perforated in many places, enabling the exchange of fluids between the two cavities.
The heart itself is a tube of annular muscles consisting of epithelial tissues, with two lateral openings (ostia) per segment. While it is not known whether the rear end is open or closed, from the front it opens directly into the body cavity. Since there are no blood vessels, apart from the fine vessels running between the muscle layers of the body wall and a pair of arteries which supply the antennae, this is referred to as an 'open circulation'.
The timing of the pumping procedure can be divided into two parts: diastole and systole. During diastole, blood flows through the ostia from the pericardial sinus (the cavity containing the heart) into the heart. When the systole begins, the ostia close and the heart muscles contract inwards, reducing the volume of the heart. This pumps the blood from the front end of the heart into the perivisceral sinus containing the organs. In this way the various organs are supplied with nutrients before the blood finally returns to the pericardial sinus via the perforations in the diaphragm. In addition to the pumping action of the heart, body movements also have an influence on circulation.
Oxygen uptake occurs to an extent via simple diffusion through the entire body surface, with the coxal vesicles on the legs possibly being involved in some species. However, of most importance is gas exchange via fine unbranched tubes, the tracheae, which draw oxygen from the surface deep into the various organs, particularly the heart. The walls of these structures, which are less than three micrometers thick in their entirety, consist only of an extremely thin membrane through which oxygen can easily diffuse. The tracheae originate at tiny openings, the spiracles, which themselves are clustered together in dent-like recesses of the outer skin, the atria. The number of 'tracheae bundles' thus formed is on average around 75 per body segment; they accumulate most densely on the back of the animal.
Unlike the arthropods, the velvet worms are unable to control the openings of their tracheae. Because the tracheae are always open, entailing considerable water loss in arid conditions. For this reason velvet worms are dependent upon habitats with high air humidity.
The digestive tract begins slightly behind the head, the mouth lying on the underside a little way from the frontmost point of the body. Here, prey can be mechanically dismembered by the mandibles with their covering of fine toothlets. Two salivary glands discharge via a common conductor into the subsequent 'throat' which makes up the first part of the front intestine. The saliva that they produce contains mucus and hydrolytic enzymes, which initiate digestion both within and outside the mouth. Historically, the salivary glands probably evolved from the waste-elimination organs known as nephridia, which are found homologously in the other body segments.
The throat itself is very muscular, serving to absorb the partially-liquified food and to pump it, via the oesophagus which forms the rear part of the front intestine, into the central intestine. Unlike the front intestine, this is not lined with a cuticula but instead consists only of a single layer of epithelial tissue, which does not exhibit conspicuous indentation as is found in other animals. On entering the central intestine, food particles are coated with a mucus-based peritrophic membrane, which serves to protect the lining of the intestine from damage by sharp-edged particles. The intestinal epithelium secretes further digestive enzymes and absorbs the released nutrients, although the majority of digestion has already taken place externally or in the mouth. Indigestible remnants arrive in the rear intestine or rectum, which is once again lined with a cuticula and which opens at the anus, located on the underside near to the rear end.
In almost every segment is a pair of elimination organs called nephridia, which are derived from coelom tissue. Each consists of a small pouch which is connected, via a flagellated conductor called a nephridioduct, to an opening at the base of the nearest leg known as a nephridiopore. The pouch is occupied by special cells called podozytes, which facilitate ultrafiltration of the blood through the partition between haemocoelom and nephridium. The composition of the urinary solution is modified in the nephridioduct by selective recovery of nutrients and water and by isolation of poison and waste materials, before it is excreted to the outside world via the nephridiopore. The most important nitrogenous elimination product is the water-insoluble uric acid; this can be excreted in solid state, with very little water. This so-called 'uricotelic' elimination mode represents an adjustment to life on land and the associated necessity of dealing economically with water.
A pair of former nephridia in the head were converted secondarily into the salivary glands, while another pair in the final segment of male specimens now serve as glands which apparently play a role in reproduction.
The entire body - including the stub feet - is littered with numerous papillae: warty protrusions which carry a mechanoreceptive bristle (responsive to mechanical stimuli) at the tip, each of which is also connected to further sensory nerve cells lying beneath. The mouth-papillae, the exits of the slime glands, probably also have a function in sensory perception. Sensory cells known as "sensills" on the "lips" or labrum respond to chemical stimuli and are known as chemoreceptors. These are also found on the two antennae, which can be regarded as the velvet worm's most important sensory organs. Except in a few (typically subterranean) species, one simply-constructed eye (ocellus) lies at the base of each antenna. This consists of a chitinous ball lens, a cornea and a retina and is connected to the brain via an optic nerve. The retina comprises numerous pigment cells and photoreceptors; the latter are easily-modified flagellated cells, whose flagellum membranes carry a photo-sensitive pigment on their surface.
Both sexes possess pairs of gonads, opening via a channel called a gonoduct into a common genital opening, the gonopore, which is located on the rear ventral side. Both the gonads and the gonoduct are derived from true coelom tissue.
In females, the two ovaries are joined in the middle and to the horizontal diaphragm. The gonoduct appears differently depending on whether the species is live-bearing or egg-laying. In the former, each exit channel divides into a slender oviduct and a roomy "womb", the uterus, in which the embryos develop. The single vagina, to which both uteri are connected, runs outward to the gonopore. In egg-laying species, whose gonoduct is uniformly constructed, the genital opening lies at the tip of a long egg-laying apparatus, the ovipositor. The females of many species also possess a sperm repository called the receptacle seminis, in which sperm cells from males can be stored temporarily or for longer periods.
Males possess two separate testes, along with the corresponding sperm vesicle (the vesicula seminalis) and exit channel (the vasa efferentia). The two vasa efferentia unite to a common sperm duct, the vas deferens, which in turn widens through the ejaculatory channel to open at the gonopore. Directly beside or behind this lie two pairs of special glands, which probably serve an auxiliary reproductive function; the rearmost glands are also known as anal glands.
A penis-like structure has so far only been found in males of the genus Paraperipatus, but has not yet been observed in action. As previously mentioned, males of many Australian species exhibit special structures on the head, which apparently take over certain tasks in transferring sperm to the females.
Distribution and habitat
Velvet worms live in tropical habitats and in the temperate zone of the Southern Hemisphere, showing a circumtropical and circumaustral distribution. Individual species are found in Central and South America; the Caribbean islands; equatorial west Africa and South Africa; northern India; Indonesia and parts of Malaysia; New Guinea; Australia and New Zealand. The entire present-day distribution reflects the likely origin of the taxon on the former supercontinent Gondwana and is referred to as a "Gondwana distribution".
All velvet worms are terrestrial (land-living) and prefer dark environments with high air humidity. They are found particularly in the rainforests of the tropics and temperate zones, where they live among moss cushions and leaf litter, under tree trunks and stones, in rotting wood or in termite tunnels. They also occur in unforested grassland, if there exist sufficient crevices in the soil into which they can withdraw during the day.
Two species live in caves, a habitat to which their ability to squeeze themselves into the smallest cracks makes them exceptionally well-adapted and in which constant living conditions are guaranteed. Since the essential requirements for cave life were probably already present prior to the settlement of these habitats, this may be described as "exaptation". Agriculture has apparently made available new habitats for velvet worms; in any case they are found in man-made cocoa and banana plantations in South America and the Caribbean
Because the danger of desiccation is greatest during the day and in dry weather, it is not surprising that velvet worms are usually most active at night and during rainy weather. Under cold or dry conditions, they actively seek out crevices in which they shift their body into a resting state. Velvet worms are negatively phototactical: they are repelled by bright light sources.
The largest measured population density is very low, at approximately ten individuals per square meter; velvet worms are often difficult to find in their natural habitat.
To move from place to place, the velvet worm crawls forward using its legs; unlike in Arthropods, both legs of a pair are moved simultaneously. Contact between the underbelly and the substrate is avoided as far as possible, the body being held clear of the ground by the stub-feet. The claws of the feet are only used on hard, rough terrain where a firm grip is needed; on soft substrates such as moss the velvet worm walks on the foot cushions at the base of the claws.
The actual locomotion is achieved less by the exertion of the leg muscles than by local changes of body length. This can be controlled using the annular and longitudinal muscles. If the annular muscles are contracted, the body cross-section is reduced and the corresponding segment stretches, since its volume must remain constant due to the incompressible behaviour of the haemocoel's liquid contents; this is the usual mode of operation of the hydraulic skeleton as also employed by other worms. Due to the stretching, the legs of the segment concerned are lifted and swung forward. Local contraction of the longitudinal muscles then shortens the appropriate segment and the legs, which are now in contact with the ground, are moved to the rear. This part of the locomotive cycle is the actual leg stroke which is responsible for forward movement. The individual stretches and contractions of the segments are coordinated by the nervous system such that contraction waves run the length of the body, each pair of legs swinging forward and then down and rearward in succession. Speeds obtained in this manner vary between approximately one millimetre and somewhat more than one centimetre per second.
Velvet worms are predatory and are able to capture animals substantially larger than themselves. Their range of prey species includes woodlice (Isopoda), termites (Isoptera), crickets (Gryllidae), book/bark lice (Psocoptera), cockroaches (Blattodea), millipedes and centipedes (Myriapoda), spiders (Araneae), various worms and even large snails (Gastropoda). They are considered an ecological equivalent of centipedes (Chilopoda).
Potential victims are sought out with the the aid of the antennae and pursued into the smallest crevices. While smaller prey are killed immediately, larger animals are first immobilised using a white, protein-rich, glue-like liquid produced by the two slime glands. This is squirted from the pores of the oral papillae over a distance of up to 30 centimetres and hardens very quickly when exposed to the air, so that the prey becomes caught in the sticky substance. This substance does not adhere to the water-repellent skin of the velvet worm, which can therefore safely approach its victim. The prey is now killed and pre-digested by the injection of toxic saliva. The sharp jaws cut the food into fine pieces before it enters the digestive tract via the mouth.
This predatory way of life is probably a consequence of the velvet worm's need to remain moist. Due to the continual risk of desiccation, often only a few hours per day are available for finding food. This leads to a strong selection for a low cost-benefit ratio, which can barely be achieved with a herbivorous diet.
Predators and parasites
The velvet worm's important predators are primarily various spiders and centipedes, along with rodents and birds such as, in Central America, the Clay-coloured Thrush (Turdus grayi). Hemprichi's Coral Snake (Micrurus hemprichii) feeds almost exclusively on velvet worms. For defence, some species roll themselves reflexively into a spiral, while they can also fight off smaller opponents by ejecting slime.
Reproduction and lifecycle
Almost all species of velvet worm reproduce sexually. The sole exception is Epiperipatus inthurni, of which no males are known to exist; reproduction is therefore parthenogenetic - taking place without the need for fertilisation.
All species are in principal sexually distinct and bear in many cases a marked sexual dimorphism: the females are usually larger than the males and have, in species where the number of legs is variable, more legs. The females of many species are fertilised only once during their lives, which leads to the fact that copulation sometimes takes place before the reproductive organs of the females are fully developed. In such cases, for example at the age of three months in Macroperipatus torquatus, the transferred sperm cells are kept in a special reservoir, where they can remain viable for longer periods.
Fertilisation takes place internally, although the mode of sperm transmission varies quite strongly. In most species, for example in the genus Peripatus, a package of sperm cells called the Spermatophore is placed into the genital opening of the female. The detailed process by which this is achieved is in most cases still unknown, a true penis having only been observed in species of the genus Paraperipatus. In many Australian species there exist dimples or special dagger- or axe-shaped structures on the head; the male of Florelliceps stutchburyae presses a long spine against the female's genital opening and probably positions its spermatophore there in this way. During the process, the female supports the male by keeping him clasped with the claws of her last pair of legs. The mating behaviour of two species of the genus Peripatopsis is particularly curious. Here, the male places two-millimetre spermatophores on the back or flanks of the female. Amoebocytes from the female's blood collect on the inside of the deposition site, and both the spermatophore's casing and the body wall on which it rests are decomposed via the secretion of enzymes. This releases the sperm cells which then move freely through the Haemocoel, penetrate the external wall of the ovaries and finally fertilise the ova. Why this self-inflicted skin injury does not lead to bacterial infections is not yet understood.
Velvet worms are found in egg-laying (oviparous), egg-live-bearing (ovoviviparous) and live-bearing (viviparous) forms.
- The first (ovipares) occur only in the family Peripatopsidae, often in regions with erratic food supply or unsettled climate. In these cases, the yolk-rich eggs measure 1.3 to 2.0 mm and are coated in a protective chitin shell. Maternal care is unknown.
- The majority of species are ovoviviparous: the medium-sized eggs, encased only by a membrane, remain in the uterus. The embryos do not receive food directly from the mother, but are supplied instead by the moderate quantity of yolk contained in the eggs - they are therefore described as lecithotrophic. The young emerge from the eggs only a short time before birth. This probably represents the velvet worm's original mode of reproduction, i.e. both oviviparous and viviparous species developed from ovoviviparous species.
- True live-bearing species are found in both families, particularly in tropical regions with a stable climate and regular food supply throughout the year. The embryos develop from eggs only micrometres in size and are nourished in the uterus by their mother, hence the description "matrotrophic". The supply of food takes place either via a secretion from the mother directly into the uterus or via a genuine tissue connection between the epithelium of the uterus and the developing embryo, known as a placenta. The former is found only outside the American continent, while the latter occurs primarily in America and the Caribbean and more rarely in the Old World. The gestation period can amount to up to 15 months, at the end of which the offspring emerge in an advanced stage of development. The embryos found in the uterus of a single female do not necessarily have to be of the same age; it is quite possible for there to be offspring at different stages of development and descended from different males.
A female can have between 1 and 23 offspring per year; development from fertilised ovum to adult takes between 6 and 17 months and does not have a larval stage. This is probably also the original mode of development. Velvet worms can live to a maximum age of 6 years.
The global conservation status of velvet worm species is difficult to estimate; many species are only known to exist at their type locality (the location at which they were first observed and described). The collection of reliable data is also hindered by low population densities, their typically nocturnal behaviour and possibly also as-yet undocumented seasonal influences and sexual dimorphism.
To date, only eleven species have been studied in sufficient detail to enable population estimates, of which three - Opistopatus roseus, Speleoperipatus spelaeus and Peripatopsis leonina - are considered critically endangered, the latter being probably already extinct. Two species - Macroperipatus insularis and Tasmanipatus anophtalmus - are assessed by the IUCN as threatened, while four further species are listed as endangered.
The primary threat comes from destruction and fragmentation of velvet worm habitat due to industrialisation, draining of wetlands and "slash and burn" for agriculture. Many species also have naturally low population densities and closely restricted geographic ranges; as a result, relatively small localised disturbances of important ecosystems can lead to the extinction of entire populations or species. Collection of specimens for universities or research institutes also plays a role on a local scale.
There is between regions a very pronounced difference in the protection afforded to velvet worms: in some countries such as South Africa there are restrictions on both collecting and exporting, while in others like Australia only export restrictions exist. Many countries offer no specific safeguards at all. Tasmania has a protection programme which is unique worldwide: one region of forest has its own "velvet worm conservation plan" which is tailored to a particular velvet worm species.
Velvet worms cannot as yet be bred in captivity. However, attempts at captive-breeding do exist, motivated not only by creation of available populations for future reintroductions to the wild, but also better to enlighten the public about the creatures and their need for protection. Their often colourful appearance and their importance in evolutionary history makes them appropriate subjects for "insect zoos", for example.
In their present forms, the velvet worms are probably very closely related to the Arthropods, a very extensive taxon which incorporates, for instance, the crustaceans, insects and arachnids. They share, amongst other things, an exoskeleton consisting of α-chitin and non-collagenous proteins; gonads and waste-elimination organs enclosed in true coelom tissue; an open blood system with a tubular heart situated at the rear; an abdominal cavity divided into pericardial and perivisceral cavities; respiration via tracheae; and similar embryonic development. Segmentation, with two body appendages per segment, is also shared. However, antennae, mandibles and oral papillae are probably not homologous to the corresponding features in arthropods, i.e. they probably developed independently.
Another closely related group are the comparitively obscure water bears (Tardigrada); however, due to their very small size, these lack some characteristics of the velvet worms and arthropods such as blood circulation and separate respiratory structures. Together, the velvet worms, arthropods and water bears form a monophyletic taxon, the Panarthropoda - i.e. the three groups collectively cover all descendants of their last common ancestor.
Due to certain similarities of form, the velvet worms were usually grouped with the water bears to form the taxon Protoarthropoda. This designation would imply that both velvet worms and water bears are not yet as highly developed as the arthropods. Modern systematic theories reject such conceptions of "primitive" and "highly developed" organisms and instead consider exclusively the historical relationships between the taxa. These relationships are not as yet fully understood but it is considered probable that the velvet worms' sister groups form a taxon designated Tactopoda, thus:
Panarthropoda |--Velvet worms (Onychophora) |--Tactopoda |--Water bears (Tardigrada) |--Arthropods (Arthropoda)
For a long time, velvet worms were also considered related to the annelids. They share, amongst other things, a worm-like body; a thin and flexible outer skin; a layered musculature; paired waste-elimination organs; as well as a simply-constructed brain and simple eyes. Decisive, however, was the existence of segmentation in both groups, with the segments showing only minor specialisation. The parapodia appendages found in annelids therefore correspond to the stump-feet of the velvet worms.
Within the Articulata concept developed by Georges Cuvier, the velvet worms therefore formed an evolutionary link between the annelids and the arthropods: worm-like precursors first developed parapodia, which then developed further into stub-feet as an intermediate link in the ultimate development of the arthropods' appendages. Due to their structural conservatism, the velvet worms were thus considered "living fossils". This perspective was expressed paradigmatically in the statement by the French zoologist A. Vandel:
- Onychophorans can be considered highly evolved annelids, adapted to terrestrial life, which announced prophetically the Arthropoda. They are a lateral branch which has endured from ancient times until today, without important modifications.
Modern taxonomy strives to avoid criteria such as "higher" and "lower" states of development or distinctions between "main" and "side" branches - only family relationships indicated by cladistic methods are considered relevant. From this point of view, several common characteristics still support the Articulata concept - segmented body; paired appendages on each segment; pairwise arrangement of waste-elimination organs in each segment; and above all, a rope-ladder-like nervous system based on a double nerve strand lying along the belly.
An alternative concept, most widely accepted today, is the so-called Ecdysozoa hypothesis. This places the Annelids and Panarthropoda in two very different groups: the former in the Lophotrochozoa and the latter in the Ecdysozoa.
Proponents of this hypothesis assume that the aforementioned similarities between Annelids and velvet worms either developed convergently, or were primitive characteristics passed unchanged from a common ancestor to both the Lophotrochozoa and Ecdysozoa. For example, in the first case the rope-ladder nervous system would have developed in the two groups independently, while in the second case it is a very old characteristic, which does not imply a particularly close relationship between the Annelids and Panarthropoda.
The Ecdysozoa concept places the velvet worms' extended family in the taxon Cycloneuralia, alongside the threadworms (Nematoda), horsehair worms (Nematomorpha) and three rather obscure groups: the mud dragons (Kinorhyncha); penis worms (Priapulida); and brush-heads (Loricifera).
Protostomia |--Ecdysozoa | |--Panarthropoda (arthropods, velvet worms, water bears) | |--Cycloneuralia (threadworms, horsehair worms and others) |--Lophotrochozoa (annelids, molluscs and others) |--others
Particularly characteristic of the Cycloneuralia is a ring of 'circumoral' nerves around the mouth opening, which the proponents of the Ecdysozoa hypothesis also recognise in modified form in the details of the nerve patterns of the Panarthropoda. Both groups also share a common skin-shedding mechanism (ecdysis) and molecular biological similarities. One problem of the Ecdysozoa hypothesis is the velvet worms' subterminal mouth position: unlike in the Cycloneuralia, the mouth is not at the front end of the body, but lies further back under the belly. However, investigations into their developmental biology, particularly regarding the development of the head nerves, suggest that this was not always the case and that the mouth was originally terminal (situated at the tip of the body). This is supported by the fossil record.
The fossil record of velvet worms includes fossils from three different periods, namely the early Cambrian and Ordovician periods, the later Carboniferous and the Tertiary Neozoic era. All the Cambrian and Ordovician forms — whose affiliation with the velvet worms is disputed — still lived in the sea, while the later species were already terrestrial.
Traditionally, all prehistoric forms were placed in a separate taxon, Xenusia, while the modern forms were designated Euonychophora. However, this classification takes no account of the actual historical connections between families and hence it is not accepted under cladistic taxonomy.
The oldest near-complete fossil specimens, denoted Lobopoda, originate from the Lower Cambrian. The most conspicuous characteristics which these species share with the modern velvet worms are the worm-like body shape and numerous stub-legs. However, in contrast, many Lobopoda exhibit numerous dorsal armour plates — the sclerita — which often cover the entire body and head. Since they taper off into long, pointed spikes, it is most likely that these served a role in defense against predators. Individual sclerita are found among the so-called "small shelly fauna" (SSF) deposits from prior to the dawn of the Cambrian epoch 543 million years ago. Therefore the Lobopoda (or rather, their direct ancestors) had already emerged in the Ediacarium period of the Neoproterozoic era, and were thus the first animals to walk on legs.
The more well-known genera include, for example, Aysheaia, which was discovered among the Canadian Burgess Shales and which is the most similar of the Lobopoda in appearance to the modern velvet worms; a pair of appendages on the head suggest the precursors of today's antennae. Xenusion was apparently able to roll itself up, spines outward, giving insight into the defensive strategies of the Lobopoda. However, by far the most famous of the Lobopoda genera is Hallucigenia, which received its scientific name from the paleontologist Simon Conway Morris on account of its bizarre appearance. Reconstructed by Conway Morris with long, stilt-like legs and mysterious fleshy dorsal protuberances, it was long considered a prime example of the way in which nature experimented with the most diverse and bizarre body designs during the Cambrian. However, further discoveries showed that this reconstruction had placed the animal upside-down: interpreting the "stilts" as dorsal spines made it clear that the fleshy "dorsal" protuberances were actually legs. This second reconstruction also exchanged the front and rear ends of the creature; only after further investigation did it turn out that Conway Morris had in fact oriented the fossils correctly in this regard.
Lobopoda fossils are found today in North America, China and northeast Europe. Due to continental drift these sites were considerably further south during the Cambrian — in the tropical and temperate regions — and corresponded at that time to the calm waters of lagoons.
The way of life of the Lobopoda is to a large extent unknown; some species were apparently carnivorous, feeding on other animals such as, for example, sponges (Porifera) or sea cucumbers (Holothuroidea) of the genus Eldonia. It is considered proven that the Lobopoda underwent moulting.
During the Cambrian there still existed a substantial degree of biodiversity, which reduced drastically during the Ordovician. The Lobopoda are considered strictly to have become extinct by the beginning of the Silurian, at the latest. The US palaeontologist Stephen Jay Gould sees this as a symptom of an extensive collapse in the biodiversity of the Cambrian, which announced the end of the "experimentation phase", although his theses are controversial.
Due to their very similar morphology, the Lobopoda were traditionally linked to the modern velvet worms; from this perspective they represented the paternal line of the taxon:
Velvet worms (Onychophora, alternatively: Lobopodia) |==various Lobopoda genera (marine, paraphyletic) |--Udeonychophora (alternatively: Onychophora) (terrestrial, comprising modern and fossil species)
Occasionally the scientific name Onychophora denotes only the terrestrial forms, while the larger group — which also includes the various Lobopoda — is then designated Lobopodia.
An important alternative view assumes that the Lobopoda instead represented the paternal line of the Panarthropoda and Tactopoda:
Panarthropoda |--Aysheaia |--N. N. |--Velvet worms (Onychophora) including extinct terrestrial forms |--N. N. |==various Lobopoda genera (paraphyletic) |--Tactopoda (water bears + arthropods)
The genus Aysheaia, which shares a particularly large number of characteristics with the modern velvet worms, therefore forms the sister-group of all other Panarthropoda, which then divide into the velvet worms and all other forms. The remaining Lobopoda species are now considered representatives of the development trend which leads to the modern water bears and arthropods. From cladistic analysis, a trend can then be ascertained towards stronger external segmentation and towards a ...
However, the result is difficult to reconcile with the Articulata concept, because it means that the annelids and arthropods must have developed their pronounced segmentation independently of one another. For the velvet worms, this would mean that the absence of clearly recognisable outward segmentation represents an original, "primitive", rather than a secondary characteristic. The second hypothesis for the systematic position of the Lobopoda therefore sits much more happily with the Ecdysozoa concept.
Four terrestrial forms of velvet worms have been described, the taxonomic position of which (in contrast to the Lobopoda) is not greatly in doubt.
It is not known when the transition to a terrestrial existence was made, but it is considered plausible that it took place between the Ordovician and late Silurian — i.e. approximately 490 to 420 million years ago — in the intertidal zone. The armour typical of the Lobopoda, if it ever existed in the ancestors of modern species, may have been lost at this point in time - the greater flexibility thus gained perhaps allowing easier movement into cramped living spaces. Various other adaptations to terrestrial life may also have emerged in the intertidal zone, such as the tracheae — which would therefore have developed independently of the insects — or the internal method of fertilisation, which would also have made the safe transfer of sperm possible despite water shortage. Only speculation is possible as to when the nephridia were converted into salivary and reproductive glands; however it is known that the prey-catching slime glands were inoperative underwater, from which it can be tentatively concluded that they were probably only developed on land, perhaps originally to ward off predators.
Wherever the transition eventually occurred, it was apparently not in an environment favourable to the formation of fossils - not a single fossil showing this development has been discovered. The species Helenodora inopinata, found in the tropics during the Carboniferous period, was very probably already terrestrial and differs very little from modern species. For this reason, and the great similarity between Lobopoda and Aysheaia, the velvet worms are considered a prime example of 'evolutionary stasis' and of a 'bradytelic' rate of evolution, where the biological structure of the entire organism is changing very slowly because strong stabilising selection restricts development trends to a narrow corridor of the morphological-anatomical "space" and does not tolerate larger deviations from the "typical" velvet worm form.
Only a single fossil from the Mesozoic era has been found, the Cretaceous species Cretoperipatus burmiticus which was found in amber from south-east Burma and dates from 100 million years ago. It can already be assigned, at a stretch, to one of the modern families - the Peripatidae.
That today's velvet worms exhibit a so-called "Gondwanan distribution" strongly suggests that their last common ancestor lived on this supercontinent. The existence of Succinipatopsis balticus, a 44 million year old species discovered in Baltic amber from the Early Eocene epoch, proves that terrestrial velvet worms also existed outside Gondwana or even the modern remains of the supercontinent. The distribution of the velvet worms must therefore once have been much wider than it is today - when and why all the non-Gondwanan species died out is unknown.
The fourth fossil species is Tertiapatus dominicanus, found in amber from the Caribbean island of Hispaniola. It is possible, but not proven, that this already belonged to one of the two modern families, the Peripatidae. The species dated from between 17 and 20 million years ago.
The slime glands can be clearly recognised in both of the Tertiary fossils, thus these must have emerged no later than this period and probably much earlier. The two Tertiary species are formally combined into the taxon Tertiapatoidea, although they probably represent only a species taxon.
The modern velvet worms form a 'monophyletic' group, incorporating all the decendants of their common ancestor. Important common derivative characteristics (synapomorphs) include, for example, the mandibles of the second body segment and the oral papillae and associated slime glands of the third; nerve strands extending along the underside with numerous cross-linkages per segment; and the special form of the tracheae.
By 2004, some 155 modern species, comprising 47 genera, had been described; the actual number of species is probably about twice this. The best-known is the type genus Peripatus, which was described as early as 1825 and which in English-speaking countries stands representative for all velvet worms.
All genera are assigned to one of two families, the distribution ranges of which do not overlap but are separated by arid areas or oceans:
- The Peripatopsidae exhibit relatively many characteristics which are perceived as original or 'primitive'. They have between 13 and 25 pairs of legs, behind or between the last of which is the genital opening (gonopore). Both oviparous and ovoviviparous, as well as genuinely viviparous species exist, although the Peripatopsidae essentially lack a placenta. Their distribution is circumaustral, encompassing Australia, Tasmania, New Zealand, New Guinea, South Africa and Chile.
- The Peripatidae exhibit a range of derivative features. They are longer, on average, than the Peripatopsidae and also have more leg pairs, numbering between 22 and 43 - the gonopore is always between the penultimate pair. There are no oviparous species - the overwhelming majority are viviparous. The females of many viviparous species develop a placenta with which to provide the growing embryo with nutrients. Distribution of the Peripatidae is restricted to the tropical and sub-tropical zones; in particular, they inhabit Central and northern South America, several Caribbean islands, West Africa, northern India, Malaysia and various Indonesian islands.
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