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Home , Arthropod, Onychophora, Peripatus

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Introduction - Onychophorans or velvet are carnivorous, terrestrial , which inhabit tropical and temperate forests of the and around the , where they are mainly found in rotted logs and leaf litter (Ruhberg 1985, Reid 1996, Mayer 2007, Oliveira et al. 2012a). So far, about 200 species of Onychophora have been described (Mayer and Oliveira 2011, 2013, Oliveira et al. 2012a, 2013a). They are classified in two subgroups, the and , which diverged prior to the break-up of Gondwana over 175 million ago (Hamer et al. 1997, Allwood et al. 2010, Braband et al. 2010, Jeffery et al. 2012, Mayer and Oliveira 2013, Murienne et al. 2014). Onychophorans have a typical - shaped body with 13–43 pairs of stumpy, unjointed (= lobopods), the number of which varies inter- or intra-specifically (Ruhberg 1985, Reid 1996, Oliveira et al. 2012a, 2012b). The anterior-most limbs have been modified to three pairs of specialized cephalic : the sensory antennae, the situated within the mouth cavity, and the slime papillae, which are used for defence and prey capture (Manton and Heatley 1937, Read and Hughes 1987, Storch and Ruhberg 1993, Mayer et al. 2010, Oliveira and Mayer 2013).

Onychophorans are predators that use a sticky slime produced in large glands and ejected via the slime papillae to entangle the prey, such as crickets and other small invertebrates (Manton and Heatley 1937, Lavallard and campiglia 1971, Ruhberg and Storch 1977, Read and Hughes 1987, Baer and Mayer 2012). After the prey has been immobilized using the glue-like slime, its is punctured with the jaws and digestive is injected into its body (Manton and Heatley 1937, Baer and Mayer 2012). The liquefied contents are then ingested using a sucking (Mayer et al. 2013a, Nielsen 2013). Besides the pharynx and the mouth cavity containing the jaws and the tongue, the digestive tract of onychophorans exhibits atubular oesophagus, followed by a thick-walled, straight midgut, and a short posterior hindgut (Balfour 1883, Lavallard 1986, Storch et al. 1988, Mayer et al. 2013a). The hindgut opens to the exterior via a terminal . The renal organs (= nephridia) of onychophorans are segmental structures that typically open to the exterior at the basis of each (Gabe 1957, Storch et al. 1978, Lavallard 1981, Mayer & Koch 2005, Mayer 2006a). The salivary, anal, uterine, and accessory genital glands, as well as the gonoducts, are generally regarded as derivatives of nephridia of the corresponding body segments (Storch et al. 1978, 1979, Reid 1996, Mayer and Koch 2005, Mayer 2006a, 2007). In , the gonoducts are associated with paired uteri that are connected to the ovarian tubes via a pair of oviducts, whereas the testes of males are associated with large (Herzberg et al. 1980, Storch and Ruhberg 1990, Storch et al. 1995, Brockmann et al. 1997, 2001, Walker et al. 2006, Mayer and tait 2009). The male and genital tracts open to the exterior via an unpaired genital opening, which is located either between the last leg pair in peripatopsids or the penultimate leg pair in peripatids (Storch and Ruhberg 1993, Oliveira et al. 2012b, Ruhberg and Mayer 2013). The body wall of onychophorans exhibits well-developed musculature consisting of an outer circular layer followed by diagonal and inner longitudinal muscle layers (Hoyle and Williams 1980). The longitudinal musculature is organized into two dorsal, two lateral, and three ventral bundles without any metameric arrangement, whereas the muscles associated with limbs are clearly segmental (Hoyle and Williams 1980, Oliveira et al. 2013b). The transverse musculature and the pericardial septum subdivide the of onychophorans (= haemocoel) into one large perivisceral sinus, two lateral sinuses, and one dorsal pericardial sinus, which contains a tube-shaped, longitudinal dorsal vessel (= ) (campiglia and Lavallard 1975, Seifert and Rosenberg 1977, nylund et al. 1988, Storch and Ruhberg 1993, Ruhberg and Mayer 2013). during embryogenesis, the haemocoel of onychophorans arises by mixocoely, i.e. a fusion of the primary and secondary (= coelomic) body cavities (von Kennel 1888, Mayer et al. 2004, 2005, Mayer 2006a).

Together with (water bears), onychophorans are regarded as the closest relatives of (, , , and allies) – the largest and most diverse groups on . However, in contrast to arthropods, the of onychophorans has changed little since the Early , rendering them important for addressing various evolutionary and other scientific questions, for example:

• How did the panarthropod ancestor look like? • What are the origins of vision and colour vision? • How are the major groups related to each other? • What is the developmental basis of animal ? • What is the phylogenetic position of tardigrades? • How did the arthropod evolve? • What are the origins of the arthropod ? • How did the mitochondrial genomes evolve? • To what extent are velvet worms useful for conservation? • What is the actual species diversity of Onychophora? • Can the onychophoran slime be used for bioengineering?

Time of origin: Onychophora evolved from the marine onychophoran-like organism pedunculata from the Mid-Cambrian period about 520 million years ago.

Zoological Importance of Onychophora: Onychophora show a great zoological importance because: 1. They furnish an example of discontinuous distribution and

2. They represent an example of living connecting link between the two phyla— Annelida and Arthropoda.

Anatomical Peculiarities of Onychophora: A. Primitive features: 1. Onychophora are worm-like body covered with thin, flexible, chitinous cuticle. 2. Onychophora are sluggish in . 3. Head segments are comparatively small (3 head segments in onychophores but in true arthropods head segments are 5 or 6). 4. Presence of segmentally arranged nephridia. 5. Presence of cilia in the reproductive tracts. 2. Onychophora are sluggish in nature. 3. Head segments are comparatively small (3 head segments in onychophores but in true arthropods head segments are 5 or 6). 4. Presence of segmentally arranged nephridia. 5. Presence of cilia in the reproductive tracts.

B. Sole peculiarities: 1. Segmentation indistinct on external surface. 2. Head appendages include a pair of antennae, a pair of jaws and a pair of oral papillae. 3. Texture of the is present. 4. Numerous, un-jointed, stumpy legs, terminated into a pair of , quite unlike the parapodia of polychaeta. 5. Tracheae and disposition of the tracheal apertures are not arthropod-like. 6. Presence of a pair of slime glands opening at the ends of the oral papillae that secrete proteinaceous adhesive substance and helps to capture the prey. 7. Lacking of . 8. Subcutaneous haemal channels.

C. Salient features: 1. -like body, ranging from 5 mm to 15 cm in length. 2. Body soft and covered by a thin, flexible, chitinous cuticle which is moulted periodically. 3. Indistinct segmentation externally and marked only by the presence of paired, un-jointed, hollow stumpy appendages (13 to 43 pairs according to species). These un-jointed walking legs are called lobopods. 4. Each walking leg terminates in a pair of curved claws. 5. Integument with fine transverse wrinkles and with numerous conical large and small tubercles. 6. Simple , similar with that of an-nelidan . 7. Head with 3 pairs of appendages including a pair of annulated antennae, a pair of -like mandibles (jaws) which are the modified 2nd pair of appendages and a pair of oral papillae (3rd pair of ). 8. A pair of slime glands are present inside the body which open to the tip of the oral papillae that discharge the adhesive material, used for to capture prey and defence. 9. Body wall dermomuscular. Muscles are un-striated. 10. Reduced . 11. Haemocoelomic body cavity. 12. Open with lateral valvular ostia on the heart. 13. Elongated tubular heart which is surrounded by pericardial sinus occurring the entire length of the body. 14. Delicate un-branched, rarely branched tracheal tubes open by means of small spiracles, scattered irregularly. Spiracles are without any closing device. 15. A single pair of nephridia in each segment except the genital opening bearing segment. 16. Ladder-like nervous system. is large, bilobed and situated dorsal to the pharynx. 17. Reproductive and excretory ducts are ciliated. 18. Dorsal coelomic . 19. separate (gonochoristic). 20. Fertilization internal. 21. Oviparous or ovoviviparous with yolky or non-yolky . 22. Viviparous with . 23. holoblastic in the eggs of viviparous species and superficial in the oviparous forms which lay their eggs in moist condition. 24. Development direct. 25. Nocturnal and carnivorous in habit.

Characters of the living families:

I. Peripatopsidae: Number of legs varies from 14-19 pairs; legs with complete spinous pads are 3; the absence of a on the inner side of the jaws; primary dermal papillae without a constriction nephridial opening on 4th and 5th pairs of legs in between third spinous pads; genital opening between or behind last pair of legs, oviparous or ovoviviparous.

II. Peripatidae: Number of legs varies from 19-43 pairs; legs with complete spinous pads 4-6; the presence of a diastema on the inner blade of the jaws; primary dermal papillae with a constriction; nephridial openings on 4th and 5th pairs of legs in between third spinous pad; genital opening in between the legs of the penultimate pair. Skin brownish, extracted by ; ovoviviparous or viviparous.

Evolutionary significance of Onychophora :

To understand why the rare and frankly esoteric velvet worm is so fascinating to evolutionary biologists, you first need to know a little bit about lagerstatten and the Cambrian Period. Lagerstatten are fossil lodes — dense assemblages of well-preserved that often shed light on the workings of entire ancient . Two lagerstatten preserve a host of strange-looking from the Cambrian Period, the evolutionary dawn of animals themselves. The in Canada, which is about 505 million years old, and the more recently discovered Chengjiang formation in , which dates to 520 million years old contain the remains of a host of odd-looking sea dwellers — and not just their hard parts, but the soft body parts of animals that would normally rot away, giving paleontologists a remarkably clear glimpse of the that inhabited Earth's ancient oceans — and it is strange view indeed! Five-eyed, fluke-like critters paddled around and hoovered up food with a clawed, tube mouth, wormy creatures armed with long, pincushion spikes wandered around the seafloor, and large, squishy animals with armored, circular mouths and jointed tusks undulated overhead.

Since the Burgess Shale was first discovered in 1909, scientists have wondered how these ancient animals connect to those alive today. Are these creatures actually close relatives of modern species (albeit, strange-looking ones) — or do these lineages represent failed evolutionary experiments, forays into body plans that didn't survive and aren't represented anywhere on Earth today? After much debate, the short answer seems to be, some are, some aren't. The five-eyed fluke, now known as ? An extinct lineage with no close, modern relatives. That pincushion worm, now called ? Well, scientists have gone back and forth on that. The first paleontologists to study creature surmised that it walked around on its spikes and had a row of waving tubes down its back. Unsurprisingly, they hypothesized that it had no modern corollaries. But in the 1990s additional fossils revealed that the tubes actually came in pairs and probably served as fleshy, tube feet, with the spikes pointed up for defense, turning the whole reconstruction of the species on its head. Further studies suggested that the mysterious Hallucigenia was actually a spiky, sea-dwelling onychophoran!

Recent investigations of Hallucigenia fossils are also consistent with this . When Canadian and British scientists used microscopes to look closely at Hallucigenia's spikes, they found that they were covered in tiny scales and constructed like stacks of very pointy ice cream cones. Since the cone-shaped jaws and claws of modern onychophorans are constructed in the same way, this trait serves as further evidence that the two lineages are closely related. It seems likely that this cone-in-cone construction of hard parts was inherited by both modern onychophorans and Hallucigenia from their common ancestor. In addition, the tiny scales and unique construction of Hallucigenia's spikes helps solve a paleontological mystery. Many sediments from the Cambrian — ones that preserve fossils less perfectly than the Burgess Shale or the Chengjiang formation — are full of mysterious tiny shells that weren't easy to identify. Now it appears that many of those shells are actually Hallucigenia spikes (minus the rest of the velvet worm) and that this creature lived not just in the ecosystems preserved in lagerstatten, but was common and lived all over the world.

Biologists are particularly interested in onychophorans because they can help us understand the of one of the most successful groups of animals ever to live on Earth: the arthropods, a clade of segmented animals with jointed legs, that includes insects, spiders, and crustaceans. Onychophorans are not arthropods — their squishy tube legs make that clear — but they do seem to be closely related to arthropods. For one thing, even though they are soft-bodied, onychophorans have to molt in order to grow, just as arthropods do. And even though they don't look segmented from the outside, some of the interior organs of an onychophoran are arranged serially, much like those of a segmented animal. Onychophorans even breathe like insects do — through a system of holes and tubes throughout their body called tracheae. Genetic also support this idea. Genetic sequences from arthropods, onychophorans, and other animals suggest that onychophorans occupy the branch of the tree of life that is right next door to that of the arthropods. The two groups are sister taxa — i.e., each others' closest relatives. Knowing which organisms occupy the branches adjacent to the arthropods' is important because it helps scientists reconstruct what the ancestors of these groups were like, and correspondingly, how modern arthropods evolved.

Onychophorans belong to a clade that has been on Earth for half-a-billion years and is closely related to arthropods. Yet these fuzzy creatures are not "precursors" to armored and . Rather, ancient onychophorans lived alongside the lineage that gave rise to arthropods and shared many traits with that ancestor. Modern onychophorans provide a window on the past, but occupy their own branch on the tree of life — one that has yet to be fully explored if the newly discovered Vietnamese species is any indication!

Is a Valid Evolutionary Intermediate?

Peripatus is an organism classified within the Onychophora, a group known as “velvet worms” or “onychophorans” (meaning “claw-bearers”). These animals live mostly in humid forests, especially in the . They hide by day under rotting logs and in leaf litter, and hunt for prey at night. The largest species is about 15 cm long. Velvet worms have between 14 and 43 pairs of stumpy, unjointed legs with claws at the tip (Starr and Taggart,; diagram below from Barnes et al.).

Onychophorans are able to capture even quite active animals such as by spraying a mucus-like substance up to half a meter from adhesive glands near their mouth. The sprayed substance hardens almost immediately on exposure to air, forming an extremely sticky meshwork that entangles the prey (Barnes et al.). As shown by the following quotations, Peripatus and onychophorans in general have often been called upon to assist the case for evolution. They are sometimes described as the “missing link” between , the phylum to which earthworms and leeches belong, and arthropods, the group including - legged animals such as , spiders, and insects (Ballard et al.). “Peripatus is a missing link between the annelids and the arthropods. It is obviously a segmented animal; its excretory, reproductive, and nervous systems are similar to those of the annelids, while its circulatory and respiratory systems are similar to those of the arthropods.” (Mader) “. . . there are all sorts of gaps [in the fossil record]: absence of gradationally intermediate transitional forms between species, but also between larger groups—between, say, families of carnivores, or the orders of mammals. In fact, the higher up the Linnaean hierarchy you look, the fewer transitional forms there seem to be. For example, Peripatus, a lobe-legged wormlike creature that haunts rotting logs in the Southern Hemisphere, appears intermediate in many respects between two of the major phyla on Earth today: the segmented worms and the arthropods. But few other phyla have such intermediates with other phyla, and when we scan the fossil record for them we find some, but basically little, help.” (Eldredge) “An animal that comes closer than any other to being the ‘missing link’ between any two phyla is the PERIPATUS, member of the small phylum Onychophora. . . .” (Buchsbaum) In contrast to such claims for Peripatus and the onychophorans, a recent college textbook on , authored by evolutionists, argues that these animals cannot be ancestral to the arthropods (Barnes et al.): “For many years, the onychophorans have been of scientific interest chiefly as living examples of a half-way stage between the worm and arthropod grades of organization. Like worms, they are soft-bodied and possess hydrostatic , ciliated excretory ducts and layers in the body wall; and, similarly to the arthropods, they bear legs, tracheae, a heart with ostia, longitudinally partitioned blood sinuses, and jaws derived from the appendages, in this case from the claws that terminate the walking legs. The precise structure of their arthropod-like features, however, strongly indicates that they have achieved them in parallel, and that whereas they illustrate what the early uniramians, for example, may have looked like, the onychophorans cannot be ancestral to any known arthropod group. Their tracheae, for instance, are simple, mostly unbranched tubes issuing many at a time from the many spiracles that are scattered over each leg-bearing ‘segment’, and their jaws, which move in the anterior/posterior plane, act independently of each other and function as ripping organs by virtue of their pointed tips rather than as chewing appcndages. Other onychophoran peculiarities include the structure of the ventral nerve cords, with their numerous connectives but without ‘segmental’ ganglia.” In agreement with the above quotation, Ballard et al. conclude “that onychophorans are a highly specialized assemblage [and not] a primitive ‘missing link’ ”. As for the overall evolutionary status of onychophorans, these authors are uncertain: “Parsimony analysis . . . suggests that onychophorans form a sister group to chelicerates (spiders and ) and crustaceans plus hexapods [insects], but this relationship is not well supported by testing. These relationships conflict with [all four major] current hypotheses of evolutionary pathways within arthropods”. Drawing on the results of Ballard et al., and other researchers, evolutionist Peter Price notes that while (from an evolutionary point of view) “the affinities among the arthropods and related groups are by no means clear,” it is nevertheless clear enough that “velvet worms are not a missing link between the arthropods and the annelids”