The phylum Onychophora, also known as 'peripatus', 'velvet worms' or 'walking worms', comprises over 180 described species. Onychophorans are exclusively terrestrial, but are susceptible to desiccation and are restricted to humid microsites. The majority of species inhabit tropical forest litter. Their flexible trunk, retractile limbs and ability to squeeze through small interstices all make them excellently adapted for life in decomposing wood and leaf litter. The head appendages are modified for form sensory antennae, slicing mandibles and slime papillae. The last are a unique trait of onychophorans and eject a rapidly polymerising glue, which is used to entangle their animal prey. Both morphological and molecular phylogenetic studies place the Onychophora at the base of the phylum Arthropoda. Gas exchange via an invaginated tracheal system and water-conserving uricotely represent show convergent evolution with similar terrestrial adaptations in insects.
Onychophorans possess typical arthropod traits: a chitinous cuticle, metameric segmentation with paired segmental limbs and periodic moulting regulated by steroid ecdysones.
Gas exchange in onychophorans is accomplished by spiracles scattered over the body surface and which open into fan-like clusters of tracheal tubules.
The flexible trunk functions as a hydrostatic skeleton, deformed by antagonising circular and longitudinal muscle layers beneath the integument.
Onychophorans possess little resistance to desiccation and are mostly confined to humid habitats in the tropics and sub-tropics.
Some species are able to take up water by eversible coxal vesicles at the leg-bases.
The anterior limbs are specialised as sensory antennae, slicing mandibles and slime papillae that eject a fast-polymerising glue to entangle prey.
Most onychophorans possess separate sexes (gonochoristic) and fertilisation involves various mechanisms of spermatophore transfer, often during an elaborate courtship.
The onychophoran body is caterpillar-like, comprising a poorly differentiated head and cylindrical trunk bearing paired, segmental appendages (Figure 1). Although species range from approximately 1 cm to over 15 cm in length, the basic body plan and anatomical features are highly conserved. Onychophorans are metamerically segmented, as are annelids and arthropods. The epidermis is overlain with a thin chitinous cuticle, and the general integument is strongly folded into transverse, circumferential ridges. These provide the trunk with remarkable capacity for deformation; Manton 1977 determined that onychophorans could squeeze through a hole one-ninth of the animal's resting cross-sectional area. The animals exploit their highly flexible integument to great effect when moving among dense litter, soil or rotting wood. See also Arthropoda (Arthropods)
The head bears a pair of long antennae and at the base of each antenna is a simple eye. Developmentally, the antennae appear homologous with the other segmental appendages. The first of these is the single pair of jaws (mandibles), which can be protruded between the oral 'lips' or buccal papillae and possess enlarged, slicing claws. Slightly posterior and lateral to the mouth is a pair of short, specialised limbs, the slime papillae, into which open the long ducts of large, arborescent slime glands. The remaining limbs consist of several pairs of lobopodial walking legs. The legs possess a thin terminal tarsus bearing small, paired claws and three broad ventral pads that provide for traction. Depending on species, the legs may number from 12 to over 40 pairs. The number of leg pairs is also variable within a given species, and females typically possess a greater number than males (Monge-Najera, 1994).
The internal anatomy of an onychophoran is, in many respects, typical of the arthropod plan (Manton, 1977; Figure 2). Below the integument lies a layer of circular muscles. These contract to lengthen the trunk and are antagonised by a longitudinal musculature organised in discrete blocks. Beneath the muscle layers is the haemocoel, which fulfils the combined roles of hydrostatic skeleton, circulatory system and frequently (in females) seminal receptacle. As in other arthropods, the blood is circulated by means of a dorsal ostiate heart that runs almost the full length of the animal. The valved ostia open under negative luminal pressure (when the heart muscle relaxes) to admit blood from the haemocoel. The gut, paired gonads and slime glands lie suspended in the haemocoel.
The onychophoran cuticle represents a protective barrier and a highly specialised tissue in its own right (Robson, 1964; Hackman and Goldberg, 1975; Storch, 1984; Wright and Luke, 1989; Figure 3). Outermost is a compound laminate epicuticle, containing a basal lipid layer, which probably serves to render the cuticle hydrofuge. Beneath this is the thick, basal procuticle of α-chitin and protein. In rigid projecting structures, such as sensory setae, spines on the ventral pads of the legs, the tarsal claws and the mandibles, the procuticle is extensively tanned. Below the cuticle is the epidermis and beneath this a thick collagen basement membrane. The collagen fibres are organised as several layers, oriented in progressively shifting angles to confer stiffness in multiple axes. This may preserve tonus and form in the integument, restoring the folded configuration following localised deformation by the hydrostatic skeleton. The basement membrane also serves to anchor the cuticle to the body wall musculature via numerous tonofibrils that traverse the epidermis. See also Chitin
Onychophorans fulfil gas exchange by a tracheal system superficially resembling that of insects and myriapods. Numerous spiracles are distributed over the general body surface (rather than being organised as segmental pairs as in insects) and these each open into a short atrium from which radiate several fine tracheae (Moseleyi, 1874). The haemolymph of one genus, Epiperipatus, has been shown to possess an arthropod-type haemocyanin blood pigment (Kusche et al., 2002), and haemocyanins may well be widespread in the phylum. They probably facilitate the transfer of oxygen from the tracheae to the tissues.
As with more familiar arthropods, the cuticle must possess modified sensilla for transducing external stimuli into action potential relays. A scanning electron micrograph of the integument reveals densely packed 'dermal papillae' lying along the folded cuticular ridges (Figure 4). The papillae are formed from several imbricate cutaneous scales and are usually surmounted by a sensory hair or seta (Wright and Luke, 1989); the overall appearance is reminiscent of an artichoke. They may be locally modified to form glandular organs such as the crural papillae, probable pheromone-secreting glands present at the base of the legs in the males of some species. The antennae bear dense arrays of long setae that are probably gustatory and tactile in function. See also Sensory Processing in Invertebrate Motor Systems
Onychophorans are susceptible to desiccation (Meyer and Eisenbeis, 1985) and even larger species lose a significant fraction of their body mass (>10%) per hour in fast-flowing, dry air (0% relative humidity (RH)), similar to the water loss incurred by an earthworm of similar mass. Approximately 34% of water loss occurs from the numerous, non-closeable, spiracles in Peripatopsis capensis (Clusella-Trullas and Chown, 2009). This arrangement appears poorly adapted for terrestrial life, but onychophorans avoid extreme desiccating environments and are largely subterranean, appearing on the ground surface only during brief nocturnal forays. In still or slowly moving air at high humidity (<0.1 ms−1; >70% RH) the spiracles, residing in deep crypts between the integumental folds, are overlain by a substantial boundary layer of water vapour and the animals lose water at comparable rates to woodlice, millipedes and hygric insects. Behaviourally, they are strongly hygrokinetic, meaning that they move up humidity gradients and become less active as the humidity approaches saturation. To offset water losses, some species are able to absorb liquid water via eversible coxal sacs at the base of the legs. The method of water uptake is incompletely understood but appears to involve a standing osmotic gradient established by the active transport of sodium and chloride into basolateral membrane invaginations of the gland epithelium (Alexander and Ewer, 1955; Lavallard and Campiglia, 1981).
An additional adaptation for water conservation is the elimination of waste nitrogen by uricotely. Rather than excreting aqueous ammonia or urea, both of which require the elimination of water at significant rates to prevent them accumulating to toxic concentrations, onychophorans excrete uric acid. Urate is transported across the gut wall but has very low solubility and precipitates in the hind gut during water resorption; it is voided as a semisolid paste with the faeces (Manton and Heatley, 1937). Uricotely is shared by reptiles, birds and insects and allows the elimination of waste nitrogen with almost no water. It is likely to be of considerable importance to onychophorans in view of their carnivorous diet and correspondingly high nitrogen turnover. See also Uric Acid Metabolism
Living chiefly in saturated microclimates can periodically present a problem of water gain rather than loss since saturated water vapour will diffuse into animal tissues down the small water activity gradient. Water gained from saturated air or prey is eliminated by segmental nephridia, coiled excretory tubules capable of excreting dilute urine, and which serve in osmotic and ionic regulation of the haemolymph. Immersion during heavy rainfall seems to present little problem to onychophorans since the hydrophobic cuticle traps a thin air film against the body surface rendering the animal unwettable. Diffusion of oxygen can continue from the water into this air film and thence into the tracheal system, providing a physical gill.
Locomotion in Onychophorans is accomplished by a variety of gaits (Manton, 1977), animals employing more legs with a shorter stride length to generate greater force at the expense of forward velocity - for example, when pushing through soil interstices. Most species are carnivorous and they feed on a wide range of soil invertebrates. Larger prey items are disabled in a remarkable way. The slime papillae are aimed at the quarry and rapid contraction of the large gland reservoir ejects a stream of rapidly hardening, proteinaceous glue (Alexander, 1957). The hardening process is accomplished by the cross-linking of disorganised proteins rather than highly structured silk-like proteins (Haritos et al., 2010). Peripatopsis moseleyi can discharge this glue over a distance of 45 cm! The immobilised victim is then attacked with the mandibles, which move alternately and slice through the body wall. The salivary glands pump digestive enzymes into the wound and the liquefied tissues of the prey are sucked in by the pumping action of the muscular pharynx. This feeding process is fundamentally similar to that of spiders.
Onychophorans have separate sexes and males produce spermatophores that are presented to the female by a variety of methods (Tait and Norman, 2001). Relatively little is known of the courtship and methods of mate attraction. In Peripatus acacioi, the male transfers a spermatophore directly from the genital opening into the female's vagina. In other species, including Peripatopsis spp., a spermatophore is deposited on the body wall of the female and elicits a breakdown of the integument, allowing the sperm to enter the haemocoel and pass to the ovary. Several genera are viviparous, brooding the developing embryos and nourishing them via a placental cord derived from the embryo sac. Probably the majority of genera, however, are ovoviviparous, brooding the eggs until shortly after hatching. A few species are oviparous, laying large yolky eggs in moist soil. The yolk reserves nourish the embryo until hatching. See also Reproduction and Life Cycles in Invertebrates
Extant species of onychophorans are mostly restricted to the former Gondwanaland continents: Africa, Australasia, Indo-China and South America; they are often cited as a group showing a relict Gondwanaland distribution. The minor morphological variation across living species makes for a relatively simple taxonomy with only two distinguished families: the Peritopsidae and Peripatidae. Most species inhabit forest litter and are seldom seen. Identification of onychophorans is complicated by intraspecific variability of such features as the number of limbs, and the number and position of crural glands and coxal vesicles. Their susceptibility to desiccation precludes dispersal across arid habitats and many populations have probably been isolated for thousands or millions of years - particularly in montane regions where altitude and local variation in rainfall can delimit forest zones quite sharply. Over 180 species of onychophorans have been described but many apparent species are actually complexes of several microspecies that have become reproductively isolated through allopatry (Oliveira et al., 2011). This makes estimates of species numbers for the phylum difficult and rather variable. The tendency for onychophorans to show limited dispersal and regionally unique traits also makes many populations vulnerable to habitat disturbances and land development (Mesibov and Ruhberg, 1991). See also Continental Drift, and Conservation of Populations and Species
To date, only a few fossil onychophorans have been found. The oldest of these is Helenodora, an animal from swamp forest remains from the middle Pennsylvanian (c. 300 million years ago (mya)) in northern Illinois (Thompson and Jones, 1980). This clearly indicates that they are an ancient group. Other fossil genera include three species described from Cretaceous and Tertiary amber. Gondwanaland did not finally separate from the Palaeozoic supercontinent Pangaea until approximately 180 mya, long after the Pennsylvanian, suggesting that the present Gondwanaland distribution of onychophorans is due to their disappearance in the northern continents and not to their originating within Gondwanaland. Given this, we can only speculate on the true age of the group. If it is assumed that the phylum originated on land - since so many onychophoran characters represent terrestrial adaptations - they may date to as early as the late Silurian or Devonian (420-350 mya) when the first forest ecosystems were diversifying. Allozyme sequence divergence indicates an ancient radiation of extant genera, and the wide distribution of both the Peritopsidae and Peripatidae across the southern continents indicates that these families diverged prior to the break-up of Gondwanaland. Clues to the marine ancestry of onychophorans may lie in the several lobopodial fossil arthropods known from the Cambrian. The most famous of these are Ayshaeia and Burgessochaeta, from the Burgess Shale of British Columbia and Xenusion from Eastern Europe. The Cambrian deposits in Chengjiang, China, have also yielded several recently described lobopodial arthropods (see Ou et al., 2011). Although these bear a superficial resemblance to onychophorans, it is presently difficult to assess their closer affinities. See also Burgess Shale, Fossil Record, and Terrestrial Ecosystems in the Past 100 Million Years
With their highly conserved body plan and narrow ecological diversity, onychophorans appear a relatively isolated group. The paired, ventral nerve cord, metameric segmentation and paired limbs, clearly place them within the Protostomia (Spiralia). Their affinities with the Arthropoda are now seldom challenged and are well supported by such characters as the α-chitin procuticle, brain structure (Strausfeld et al., 2006), haemocoel and arthropod-type haemocyanins. Molecular sequence data from 12S ribosomal ribonucleic acid (rRNA) provides further evidence that onychophorans are arthropods (Ballard et al., 1992; Giribet et al., 1996, 2001; Regier et al., 2010). Molecular phylogenetic studies, including sequence analyses of arthropod haemocyanin genes (Kusche et al., 2002), have repeatedly placed the Onychophora within the Arthropoda but outside the 'Euarthropoda' (myriapods, crustaceans, hexapods and chelicerates). The other arthropodan taxon showing basal affinities with the arthropods is the Tardigrada. All three groups (Onychophora, Tardigrada and Euarthropoda) are, however, separated by large genetic distances, indicating an ancient divergence and obscuring their actual affinities. See also Molecular Phylogeny Reconstruction, Myriapoda (Including Centipedes and Millipedes), and Tardigrada
Current molecular phylogeny indicates that arthropods and annelids belong to two distinct superphyla within the Protostomia - the Ecdysozoa and Lophotrochozoa, respectively (Peterson and Eernisse, 2001; Giribet, 2008). This argues against a close affinity between onychophorans and annelids.
The geographic separation of populations creating barriers to gene flow and thus potentially leading to genetic divergence over time. Most speciation in animals is believed to involve allopatry.Blood pigment
A protein, often complexed with porphyrin molecules, that binds oxygen via a metal ion (copper or iron) and increases the oxygen that can be carried in blood or other tissues. The commonest forms are haemoglobins (using iron) and haemocyanins (using copper). Depending on oxygen affinity, blood pigments can allow aerobic metabolism in oxygen-depleted environments.Chitinous
Containing the stiff polysaccharide chitin (poly n-acetyl glucosamine); the α-chitin procuticle is a probable derived character of the Arthropoda.Gondwanaland
One of the two Mesozoic supercontinents (the other being Laurasia) that separated from the single Palaeozoic supercontinent Pangaea approximately 180 mya. Gondwanaland comprised present-day Indo-China, sub-Saharan Africa, South America and Australasia, and began to break up over 60 mya.Haemocoel
The open blood system of arthropods and molluscs comprising a system of sinuses. It is formed from the embryonic union of the haemal and coelomic systems in arthropods.Parsimony analysis
The reconstruction of phylogenetic trees from data such as base-pair sequences involving the clustering of taxa into dichotomously branching groups so as to minimise the number of derived (new) evolutionary events (e.g. base-pair changes) required to account for the observed differences.Protostomes
A group of phyla including the Annelida, Arthropoda and Mollusca (and several smaller phyla), sharing several fundamental characters including paired ventral nerve cords, spiral determinate cleavage, embryonic protostomy (blastopore becomes the mouth), mesoderm derived from the 4d cell, and planktonic larvae (when present) of the trochophore type. Molecular phylogenetic methods reveal two major radiations within the protostomes: the Ecdysozoa (including arthropods and nematodes), and the Lophotrochozoa (including annelids and molluscs).Spermatophore
A sperm package, consolidated by protein or polysaccharide and transferred from male to female; use of spermatophores circumvents copulation in several taxa.Tardigrada
A small phylum of minute, lobopodial arthropods with four pairs of limbs and piercing mouthparts for feeding on plant and animal fluids. Most species are meiofaunal and many inhabit ephemeral water in soil and epiphytes, surviving drought by cryptobiosis.Uricotely
The excretion of waste nitrogen as uric acid, an aromatic purine compound with low solubility in water, which therefore precipitates at relatively low concentrations. The whitish paste of bird excreta is uric acid. This provides a water-conserving though metabolically expensive alternative to ammonia excretion (ammonotely).
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