Onychophora

(Onychophorans, velvet worms, and peripatus)

Phylum Onychophora

Number of families 2

Thumbnail description
Terrestrial carnivorous worms with legs along the whole length of the body, paired eyes, a conspicuous pair of antennae, and a velvety appearance

Evolution and systematics

A number of fossils have been linked to the Onychophora, but whether they really fit into this group is not known with certainty. Aysheaia pedunculata from the Middle Cambrian Burgess shale has many morphological similarities with extant onychophorans, but it differs fundamentally in having a terminal mouth. Another, possibly related, fossil is the Middle Pennsylvanian Mazon Creek Helenodora inopinata, which could have been marine or terrestrial. The connection between Priapulida (based on the fossil Xenusion from the Cambrian sandstone in Germany) and Onychophora is highly speculative. However, the marine Cambrian forms (e.g., Microdictyon, Hallucigenia, and Luolishania) have been definitely assigned to the Onychophora by some authors.

Although first mistakenly described in 1826 as a type of slug, the evolutionary history of onychophorans has long fascinated scientists. Onychophorans were thought to be a "missing link" between the Annelids (segmented worms) and the Arthropods (a group that includes the insects and spiders) because they share morphological characters with both these large phyla. However, molecular studies show that they are, in fact, more closely related to the arthropods. Because of their many unique characteristics, they are considered a separate phylum.

Two families, the Peripatopsidae and the Peripatidae, are recognized. It is assumed that the two families are sister taxa, but whether each family is a monophyletic group (evolved from a common ancestor) has yet to be determined. Compared to many other invertebrates, the gross morphology of the Onychophora is remarkably similar over its wide and disjunct geographical range. The lack of distinguishing features has precluded a satisfactory higher-level classification and also causes difficulties at the species level, with cryptic species being common. No subfamilies are recognized.

Physical characteristics

The basic body structure of onychophorans is a simple one, but it is a design that works well. They have changed little in appearance over the last 500 million years. Onychophorans have a soft and flexible cylindrical body that is slightly flattened on the ventral side. The head bears a pair of annulated antennae with beady eyes located at their bases and a ventral circular mouth, equipped with fleshy lips and paired jaws. On either side of the mouth is an oral tube, sometimes called the "oral papillae." Paired legs, the oncopods, extend along the full length of the body and vary in number (depending on the species) from 13 to 43 pairs. The genital opening is on the ventral side at the posterior end of the body, and they have a terminal anus. Each oncopod is a conical, unjointed appendage with a foot that bears a pair of terminal claws. There are three to six spinous pads on the underside of each oncopod at the base of the feet, and often in males a crural, or pheromonesecreting, gland on the underside of some or all of the oncopods, close to their junction with the body. The body is covered by a thin cuticle that is molted at regular intervals. The cuticle is adorned with papillae, each composed of overlapping rows of scales. The largest papillae bear sensory

bristles. It is these sensory papillae that give onychophorans their velvety appearance and common name, "velvet worms."

Apart from a few white, cave-dwelling species, they are generally blue-gray or brownish in color, often intricately and beautifully patterned, with stripes, diamonds, spots, or chevrons.

Distribution

With the exception of Antarctica, Europe, and North America, extant onychophorans are found on all continents. The peripatids inhabit tropical America, and have also been found in tropical western Africa and southeastern Asia. Peripatopsids are found in countries associated with the previously connected southern super-continent, Gondwana, such as Chile, South Africa, Australia, New Guinea, and New Zealand. Their present distribution is patchy. In the northern hemisphere, the Onychophora are now restricted to tropical and subtropical regions, although fossil evidence suggests that they were much more widespread throughout Pangaea. The ancestors of peripatus moved from the sea to the land more than 400 million years ago.

Habitat

All onychophorans are confined to moist, humid micro-habitats, such as tropical and subtropical forests, where they live in leaf litter or under stones, logs, or in the soil. During dry periods, or at low temperatures, some species migrate vertically within soil crevices and remain inactive until conditions improve.

Behavior

Velvet worms exhibit photonegative behavior, which means they hide from light and respond to air movements. These reactions make it difficult to observe their behavior, so very little is known about them. Covered with sensory bristles considered to be mechanoreceptors, onychophorans are highly sensitive to touch. This is undoubtedly the primary way in which they experience their environment, and touch probably also plays a significant role in sexual activity.

Feeding ecology and diet

Onychophora are carnivorous, and feed primarily on arthropods. They capture their prey by entangling it in threads of clear, sticky slime that is ejected from the oral tubes on either side of the head.

Very little is known about the feeding ecology of onychophorans in their natural environment. The slime is also used to deter predators and may be ejected up to 1.6 ft (0.5m) in distance. In addition to other invertebrates, predators of onychophorans include birds and reptiles.

Reproductive biology

Female onychophorans are attracted to males by pheromonal secretions extruded from the males' crural glands. Reproduction takes place in an extremely curious manner. In some species, the males deposit packets of sperm (spermatophores) directly into the genital opening of the female, but in other species the spermatophores are placed somewhere on the body of the female. The skin tissue then collapses where the spermatophores are deposited, and the sperm migrate into the female's body, where they penetrate the ovaries to fertilize the eggs, or are stored for future use in paired sperm receptacles. Stored sperm remains viable for many months.

In some Australian species, the males place their spermatophores on their heads like tiny trophies in readiness to present them to a female. Some species have developed elaborate structures on their heads, including spikes, spines, hollow stylets, pits, and depressions, to either hold the sperm or assist in its transfer to the female. Mating has been observed in only a few species.

Embryonic development is extremely diverse. Some species lay large, yolk-filled eggs, while others retain yolky eggs within the female until they are ready to hatch. Some other species have small eggs without a yolky food source, and the young are retained in the body and obtain nourishment from the mother's body in a manner similar to that of placental mammals. In all species, the young are fully developed when born and, apart from lacking complete pigmentation, look like miniature adults. There is no parental care and the young forage independently soon after birth. Some species appear to give birth throughout the year, but seasonality has been recorded for other species.

Conservation status

The 2002 IUCN Red Lists includes 11 onychophoran species: three as Extinct; one as Critically Endangered; three as Endangered; two as Vulnerable; one as Lower Risk/Near Threatened; and one as Data Deficient. Because onychophorans are restricted to humid, cryptic habitats, they are highly susceptible to habitat disturbance, particularly deforestation. In some parts of the world, their relatively small populations could be endangered by excessive collecting. The very restricted distributions of many species also make them vulnerable to habitat alteration, and the destruction of indigenous forests will undoubtedly result in the extinction of many species. Most threats are a direct result of habitat disturbance by humans, including land clearing, pollution, and over-collecting.

Significance to humans

The Onychophora are excellent tools for biological research, being especially valuable for the study of evolution, phylogenetics, reproductive biology, physiology, discontinuous distribution, and continental drift.

Species accounts

List of Species

No common name

Epiperipatus biolleyi

order

No order designation

family

Peripatidae

taxonomy

Epiperipatus biolleyi Bouvier, 1902, Costa Rica.

other common names

None known.

physical characteristics

No modification of head papillae for reproduction. Number of oncopods variable, 30 pairs in females, 26–28 pairs in males; two anterior and one posterior distal foot papillae; nephridiopore (dome-shaped urinary opening) between third and fourth spinous foot pad. Gonopore (genital opening) between penultimate pair of oncopods. Crural papillae present in males, opening at base of fourth last pair of oncopods. Anterior accessory gland papillae (function unknown) in males open at base of third last oncopod pair, posterior accessory glands open on anal segment. Females without spermathecae. Viviparous, young are fully developed when born. Body sienna brown or dusky pink with dark gray papillae and mid-dorsal line. Antennae and legs gray. Up to 2 in (52 mm) in length (males); 1.5 in (38 mm) in females (measured when walking).

distribution

The species occurs in Costa Rica.

habitat

Found at densities of 0.25 individuals per m² in sandy soil with an average humidity of 35% and pH 5.2–6.2, and under and inside rotting logs and microcaverns in the soil. They occur both in low montane moist forest and in areas that have been converted to pasture.

behavior

They avoid light at around 470–600 nanometers. Walking speed is around 0.4 in (1 cm) per second. In nature, these animals often carry scars and mutilated oncopods.

feeding ecology and diet

Little is known about diet and feeding ecology in the wild.

reproductive biology

Ultrastructural examination of the female genital system has shown that insemination occurs directly via the genital opening. The species is viviparous; the young are fully developed when born.

conservation status

Not listed by the IUCN.

significance to humans

None known.

No common name

Cephalofovea tomahmontis

order

No order designation

family

Peripatopsidae

taxonomy

Cephalofovea tomahmontis Ruhberg et al., 1988, Mt. Tomah, New South Wales, Australia.

other common names

None known.

physical characteristics

Thirty antennal rings, each with single row of bristles. Male with an eversible head structure consisting of dome-shaped, fleshy crown. Distal half of the crown has rounded, scaled papillae mediodorsally. Proximal part of crown unpigmented, with scattered, pigmented papillae. When inverted, the structure forms a depression, or pit. Female head papillae modified, reduced in size and crowded together in shallow pit. Fifteen pairs of oncopods in both sexes. Crural papillae present only on first pair, or first two pairs, of oncopods. Repeated Y-shaped segmental body pattern. Up to about 2 in (50 mm) in length, with females larger than males.

distribution

The species is found in the Blue Mountains, west of Sydney, NSW, Australia, from Mt. Tomah to Mt. Wilson.

habitat

Found in and under rotting logs and among leaf litter in eucalypt forest.

behavior

They are highly secretive, so little is known about their behavior.

feeding ecology and diet

Little is known about their feeding ecology and diet. In captivity, they feed readily on slaters and Drosophilia.

reproductive biology

Males have been found with spermatophores cupped within their partially everted head structure. Mating has not been observed. This species is ovoviviparous. Females give birth to fully developed young.

conservation status

Not listed by the IUCN. This species can only be distinguished from its congeners using molecular methods, and the extent of its distribution range is not known. However, its status would seem to be secure at present.

significance to humans

None known.

Resources

Books

Storch, Volker, and Hilke Ruhberg. "Onychophora." In Microscopic Anatomy of Invertebrates. Vol. 12, Onychophora, Chilopoda and Lesser Protostomata, edited by Frederick W. Harrison and Mary E. Rice. New York: Wiley-Liss, 1993.

Periodicals

Brockman, C., R. Mummert, H. Ruhberg, and V. Storch. "Ultrastructural Investigations of the Female Genital System of Epiperipatus biolleyi (Bouvier, 1902) (Onychophora, Peripatidae)." Acta Zoologica 80 (1999): 339–349.

Elliot, S., N. N. Tait, and D. A. Briscoe. "A Pheromonal Function for the Crural Glands of the Onychophoran Cephalofovea tomahmontis (Onychophora: Peripatopsidae)." Journal of Zoology (London) 231 (1993): 1–9.

Monge-Nágera, J., and J. P. Alfaro. "Geographic Variation of Habitats in Costa Rican Velvet Worms (Onychophora: Peripatidae)." Biogeographica 71, no. 3 (1995): 97–108.

Monge-Nágera, J., Z. Barrientos, and F. Aguilar. "Behavior of Epiperipatus biolleyi (Onychophora: Peripatidae) Under Laboratory Conditions." Revista de Biologia Tropical 41, no. 3 (1993): 689–696.

Reid, A. L. "A Review of the Peripatopsidae (Onychophora) in Australia, with Descriptions of New Genera and Species, and Comments on Peripatopsid Relationships." Invertebrate Taxonomy 10, no. 4 (1996): 663–936.

Reid, A. L., N. N. Tait, and D. A. Briscoe. "Morphological, Cytogenetic and Allozymic Variation Within Cephalofovea (Onychophora: Peripatopsidae) with Descriptions of Three New Species." Zoological Journal of the Linnean Society (London) 114 (1995): 115–138.

Storch, V., R. Mummert, and H. Ruhberg. "Electron Microscopic Observations on the Male Genital Tract, Sperm Development, Spermatophore Formation, and Capacitation in Epiperipatus biolleyi (Bouvier) (Peripatidae, Onychophora)." Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut 92 (1995): 365–379.

Sunnucks, P., and N. Tait. "Tales of the Unexpected." Nature Australia 27, no. 1 (2001): 60–69.

Amanda Louise Reid, PhD