Millipede

The higher-level classification of millipedes is presented below, based on Shear, 2011,[3] and Shear & Edgecombe, 2010[9] (extinct groups). Recent cladistic and molecular studies have challenged the traditional classification schemes above, and in particular the position of the orders Siphoniulida and Polyzoniida is not yet well established.[5] The placement and positions of extinct groups (†) known only from fossils is tentative and not fully resolved.[5][9] After each name is listed the author citation: the name of the person who coined the name or defined the group, even if not at the current rank.

Class Diplopoda de Blainville in Gervais, 1844

• Subclass Penicillata Latreille, 1831
  • Order Polyxenida Verhoeff, 1934
• Subclass †Arthropleuridea (placed in Penicillata by some authors)[9]
  • Order †Arthropleurida Waterlot, 1934
  • Order †Eoarthropleurida Shear & Selden, 1995
  • Order †Microdecemplicida Wilson & Shear, 2000
• Subclass Chilognatha Latrielle, 1802
  • Order †Zosterogrammida Wilson, 2005 (Chilognatha incertae sedis)[9]
  • Infraclass Pentazonia Brandt, 1833
    • Order †Amynilyspedida Hoffman, 1969
    • Superorder Limacomorpha Pocock, 1894
      • Order Glomeridesmida Cook, 1895
    • Superorder Oniscomorpha Pocock, 1887
      • Order Glomerida Brandt, 1833
      • Order Sphaerotheriida Brandt, 1833
  • Infraclass Helminthomorpha Pocock, 1887
    • Superorder †Archipolypoda Scudder, 1882
      • Order †Archidesmida Wilson & Anderson 2004
      • Order †Cowiedesmida Wilson & Anderson 2004
      • Order †Euphoberiida Hoffman, 1969
      • Order †Palaeosomatida Hannibal & Krzeminski, 2005
    • Order †Pleurojulida Schneider & Werneburg, 1998 (possibly sister to Colobognatha)[5]
    • Subterclass Colobognatha Brandt, 1834
      • Order Platydesmida Cook, 1895
      • Order Polyzoniida Cook, 1895
      • Order Siphonocryptida Cook, 1895
      • Order Siphonophorida Newport, 1844
    • Subterclass Eugnatha Attems, 1898
      • Superorder Juliformia Attems, 1926
        • Order Julida Brandt, 1833
        • Order Spirobolida Cook, 1895
        • Order Spirostreptida Brandt, 1833
        • Superfamily †Xyloiuloidea Cook, 1895 (Sometimes aligned with Spirobolida)[10]
      • Superorder Nematophora Verhoeff, 1913
        • Order Callipodida Pocock, 1894
        • Order Chordeumatida Pocock 1894
        • Order Stemmiulida Cook, 1895
        • Order Siphoniulida Cook, 1895
      • Superorder Merocheta Cook, 1895
        • Order Polydesmida Pocock, 1887

Millipedes are among the first animals to have colonised land during the Silurian period.[11] Early forms probably ate mosses and primitive vascular plants. There are two major groups of millipedes whose members are all extinct: the Archipolypoda ("ancient, many-legged ones") which contain the oldest known terrestrial animals, and Arthropleuridea, which contain the largest known land invertebrates. The earliest known land creature, Pneumodesmus newmani, was a 1 cm (0.4 in) long archipolypodan that lived 428 million years ago in the upper Silurian, and has clear evidence of spiracles (breathing holes) attesting to its air-breathing habits.[9][12] During the Upper Carboniferous (340 to 280 million years ago), Arthropleura became the largest known land-dwelling invertebrate on record, reaching lengths of at least 2 m (6 ft 7 in).[13] Millipedes also exhibit the earliest evidence of chemical defence, as some Devonian fossils have defensive gland openings called ozopores.[9] Millipedes, centipedes, and other terrestrial arthropods attained very large sizes in comparison to modern species in the oxygen-rich environments of the Devonian and Carboniferous periods, and some could grow larger than one metre. As oxygen levels lowered through time, arthropods became smaller.[14]

Octoglena sierra (Colobognatha, Polyzoniida)

Anadenobolus monilicornis (Juliformia, Spirobolida)

Harpaphe haydeniana (Polydesmida)

The history of scientific millipede classification began with Carl Linnaeus, who in his 10th edition of Systema Naturae, 1758, named seven species of Julus as "Insecta Aptera" (wingless insects).[15] In 1802, the French zoologist Pierre André Latreille proposed the name Chilognatha as the first group of what are now the Diplopoda, and in 1840 the German naturalist Johann Friedrich von Brandt produced the first detailed classification. The name Diplopoda itself was coined in 1844 by the French zoologist Henri Marie Ducrotay de Blainville. From 1890 to 1940, millipede taxonomy was driven by relatively few researchers at any given time, with major contributions by Carl Attems, Karl Wilhelm Verhoeff and Ralph Vary Chamberlin, who each described over 1,000 species, as well as Orator F. Cook, Filippo Silvestri, R. I. Pocock, and Henry W. Brölemann.[5] This was a period when the science of diplopodology flourished: rates of species descriptions were on average the highest in history, sometimes exceeding 300 per year.[4]

In 1971, the Dutch biologist C. A. W. Jeekel published a comprehensive listing of all known millipede genera and families described between 1758 and 1957 in his Nomenclator Generum et Familiarum Diplopodorum, a work credited as launching the "modern era" of millipede taxonomy.[16][17] In 1980, the American biologist Richard L. Hoffman published a classification of millipedes which recognized the Penicillata, Pentazonia, and Helminthomorpha,[18] and the first phylogenetic analysis of millipede orders using modern cladistic methods was published in 1984 by Henrik Enghoff of Denmark.[19] A 2003 classification by the American myriapodologist Rowland Shelley is similar to the one originally proposed by Verhoeff, and remains the currently accepted classification scheme (shown below), despite more recent molecular studies proposing conflicting relationships.[5][9] A 2011 summary of millipede family diversity by William A. Shear placed the order Siphoniulida within the larger group Nematophora.[3]

In addition to the 16 living orders, there are 9 extinct orders and one superfamily known only from fossils. The relationship of these to living groups and to each other is controversial. The extinct Arthropleuridea was long considered a distinct myriapod class, although work in the early 21st century established the group as a subclass of millipedes.[20][21][22] Several living orders also appear in the fossil record. Below are two proposed arrangements of fossil millipede groups.[5][9] Extinct groups are indicated with a dagger (†). The extinct order Zosterogrammida, a chilognath of uncertain position,[9] is not shown.

Pauropods are thought to be the closest relative of millipedes.

Although the relationships of millipede orders are still the subject of debate, the class Diplopoda as a whole is considered a monophyletic group of arthropods: all millipedes are more closely related to each other than to any other arthropods. Diplopoda is a class within the arthropod subphylum Myriapoda, the myriapods, which includes centipedes (class Chilopoda) as well as the lesser-known pauropods (class Pauropoda) and symphylans (class Symphyla). Within myriapods, the closest relatives or sister group of millipedes has long been considered the pauropods, which also have a collum and diplosegments.[5]

The differences between millipedes and centipedes are a common question from the general public.[23] Both groups of myriapods share similarities, such as long, multi-segmented bodies, many legs, a single pair of antennae, and the presence of postanntennal organs, but have many differences and distinct evolutionary histories, as the most recent common ancestor of centipedes and millipedes lived around 450 to 475 million years ago in the Silurian.[24] The head alone exemplifies the differences; millipedes have short, elbowed antennae for probing the substrate, a pair of robust mandibles and a single pair of maxillae fused into a lip; centipedes have long, threadlike antennae, a pair of small mandibles, two pairs of maxillae and a pair of large poison claws.[25]

A representative millipede and centipede (not necessarily to scale)

The head of a millipede is typically rounded above and flattened below and bears a pair of large mandibles in front of a plate-like structure called a gnathochilarium ("jaw lip").[5] The head contains a single pair of antennae with seven or eight segments and a group of sensory cones at the tip.[5] Many orders also possess a pair of sensory organs known as the Tömösváry organs, shaped as small oval rings posterior and lateral to the base of the antennae. Their function is unknown,[5] but they also occur in some centipedes, and are possibly used to measure humidity or light levels in the surrounding environment.[29]

Millipede eyes consist of several simple flat-lensed ocelli arranged in a group or patch on each side of the head. These patches are also called ocular fields or ocellaria. Many species of millipedes, including the entire orders Polydesmida, Siphoniulida, Glomeridesmida, Siphonophorida and Platydesmida, and cave-dwelling millipedes such as Causeyella and Trichopetalum, had ancestors that could see but have subsequently lost their eyes and are blind.[26]

Paranota of polydesmidan (left) and platydesmidan millipedes

Millipede bodies may be flattened or cylindrical, and are composed of numerous metameric segments, each with an exoskeleton consisting of four chitinous plates: a single plate above (the tergite), one at each side (pleurites), and a plate on the underside (sternite) where the legs attach. In many millipedes, such as Merocheta and Juliformia, these plates are fused to varying degrees, sometimes forming a single cylindrical ring. The plates are typically hard, being impregnated with calcium salts.[27] Because they can't close their permanently open spiracles and most species lack a waxy cuticle, millipedes are susceptible to water loss and with a few exceptions must spend most of their time in moist or humid environments.[30]

The first segment behind the head is legless and known as a collum (from the Latin for neck or collar). The second, third, and fourth body segments bear a single pair of legs each and are known as "haplosegments" (the three haplosegments are sometimes referred to as a "thorax"[12]). The remaining segments, from the fifth to the posterior, are properly known as diplosegments or double segments, formed by the fusion of two embryonic segments. Each diplosegment bears two pairs of legs, rather than just one as in centipedes. In some millipedes, the last few segments may be legless. The terms "segment" or "body ring" are often used interchangeably to refer to both haplo- and diplosegments. The final segment is known as the telson and consists of a legless preanal ring, a pair of anal valves (closeable plates around the anus), and a small scale below the anus.[5][27]

Millipedes in several orders have keel-like extensions of the body-wall known as paranota, which can vary widely in shape, size, and texture; modifications include lobes, papillae, ridges, crests, spines and notches.[2] Paranota may allow millipedes to wedge more securely into crevices, protect the legs, or make the millipede more difficult for predators to swallow.[31]

The legs are composed of seven segments, and attach on the underside of the body. The legs of an individual are generally rather similar to each other, although often longer in males than females, and males of some species may have a reduced or enlarged first pair of legs.[32] The most conspicuous leg modifications are involved in reproduction, discussed below. Despite the common name, no millipede has been discovered with 1,000 legs: common species have between 34 and 400 legs, and the record is held by Illacme plenipes, with individuals possessing up to 750 legs – more than any other creature on Earth.[33]

A female Illacme plenipes with 618 legs (309 pairs)

Millipedes breathe through two pairs of spiracles located ventrally on each segment near the base of the legs.[23] Each opens into an internal pouch, and connects to a system of tracheae. The heart runs the entire length of the body, with an aorta stretching into the head. The excretory organs are two pairs of malpighian tubules, located near the mid-part of the gut. The digestive tract is a simple tube with two pairs of salivary glands to help digest the food.[27]

Millipedes occur on all continents except Antarctica, and occupy almost all terrestrial habitats, ranging as far north as the Arctic Circle in Iceland, Norway, and Central Russia, and as far south as Santa Cruz Province, Argentina.[39][40] Typically forest floor dwellers, they live in leaf litter, dead wood, or soil, with a preference for humid conditions. In temperate zones, millipedes are most abundant in moist deciduous forests, and may reach densities of over 1,000 individuals per square metre. Other habitats include coniferous forests, caves, and alpine ecosystems.[23][40] Deserticolous millipedes, species evolved to live in the desert, like Orthoporus ornatus, may show adaptations like a waxy epicuticle and the ability of water uptake from unsaturated air.[41] Some species can survive freshwater floods and live submerged underwater for up to 11 months.[42][43] A few species occur near the seashore and can survive in somewhat salty conditions.[34][44]

The diplosegments of millipedes have evolved in conjunction with their burrowing habits, and nearly all millipedes adopt a mainly subterranean lifestyle. They use three main methods of burrowing; bulldozing, wedging and boring. Members of the orders Julida, Spirobolida and Spirostreptida, lower their heads and barge their way into the substrate, the collum being the portion of their exoskeleton that leads the way. Flat-backed millipedes in the order Polydesmida tend to insert their front end, like a wedge, into a horizontal crevice, and then widen the crack by pushing upwards with their legs, the paranota in this instance constituting the main lifting surface. Boring is used by members of the order Polyzoniida. These have smaller segments at the front and increasingly large ones further back; they propel themselves forward into a crack with their legs, the wedge-shaped body widening the gap as they go. Some millipedes have adopted an above-ground lifestyle and lost the burrowing habit. This may be because they are too small to have enough leverage to burrow, or because they are too large to make the effort worthwhile, or in some cases because they move relatively fast (for a millipede) and are active predators.[2]

Most millipedes are detritivores and feed on decomposing vegetation, feces, or organic matter mixed with soil. They often play important roles in the breakdown and decomposition of plant litter: estimates of consumption rates for individual species range from 1 to 11 percent of all leaf litter, depending on species and region, and collectively millipedes may consume nearly all the leaf litter in a region. The leaf litter is fragmented in the millipede gut and excreted as pellets of leaf fragments, algae, fungi, and bacteria, which facilitates decomposition by the microorganisms.[32] Where earthworm populations are low in tropical forests, millipedes play an important role in facilitating microbial decomposition of the leaf litter.[2] Some millipedes are herbivorous, feeding on living plants, and some species can become serious pests of crops. Millipedes in the order Polyxenida graze algae from bark, and Platydesmida feed on fungi.[5] A few species are omnivorous or in Callipodida and Chordeumatida occasionally carnivorous,[45] feeding on insects, centipedes, earthworms, or snails.[27][46] Some species have piercing mouth parts that allow them to suck up plant juices.[23]

A Sceliages beetle transporting a millipede carcass

Millipedes are preyed on by a wide range of animals, including various reptiles, amphibians, birds, mammals, and insects.[5] Mammalian predators such as coatis and meerkats roll captured millipedes on the ground to deplete and rub off their defensive secretions before consuming their prey,[47] and certain poison dart frogs are believed to incorporate the toxic compounds of millipedes into their own defences.[48] Several invertebrates have specialised behaviours or structures to feed on millipedes, including larval glowworm beetles,[49] Probolomyrmex ants,[50] chlamydephorid slugs,[51] and predaceous dung beetles of the genera Sceliages and Deltochilum.[52][53] A large subfamily of assassin bugs, the Ectrichodiinae with over 600 species, has specialized in preying upon millipedes.[54] Parasites of millipedes include nematodes, phaeomyiid flies, and acanthocephalans.[5] Nearly 30 fungal species of the order Laboulbeniales have been found growing externally on millipedes, but some species may be commensal rather than parasitic.[55]

Ammodesmus nimba from Guinea, West Africa, curled in a defensive coil

Due to their lack of speed and their inability to bite or sting, millipedes' primary defence mechanism is to curl into a tight coil – protecting their delicate legs inside an armoured exoskeleton.[56]

Many species also emit various foul-smelling liquid secretions through microscopic holes called ozopores (the openings of "odoriferous" or "repugnatorial glands"), along the sides of their bodies as a secondary defence. Among the many irritant and toxic chemicals found in these secretions are alkaloids, benzoquinones, phenols, terpenoids, and hydrogen cyanide.[57][58] Some of these substances are caustic and can burn the exoskeleton of ants and other insect predators, and the skin and eyes of larger predators. Primates such as capuchin monkeys and lemurs have been observed intentionally irritating millipedes in order to rub the chemicals on themselves to repel mosquitoes.[59][60][61] Some of these defensive compounds also show antifungal activity.[62]

The bristly millipedes (order Polyxenida) lack both an armoured exoskeleton and odiferous glands, and instead are covered in numerous bristles that in at least one species, Polyxenus fasciculatus, detach and entangle ants.[63]

Psammodesmus bryophorus camouflaged with symbiotic mosses

Some millipedes form mutualistic relationships with organisms of other species, in which both species benefit from the interaction, or commensal relationships, in which only one species benefits while the other is unaffected. Several species form close relationships with ants, a relationship known as myrmecophily, especially within the family Pyrgodesmidae (Polydesmida), which contains "obligate myrmecophiles", species which have only been found in ant colonies. More species are "facultative myrmecophiles", being non-exclusively associated with ants, including many species of Polyxenida that have been found in ant nests around the world.[64]

Many millipede species have commensal relationships with mites of the orders Mesostigmata and Astigmata. Many of these mites are believed to be phoretic rather than parasitic, which means that they use the millipede host as a means of dispersal.[65][66]

A novel interaction between millipedes and mosses was described in 2011, in which individuals of the newly discovered Psammodesmus bryophorus was found to have up to ten species living on its dorsal surface, in what may provide camouflage for the millipede and increased dispersal for the mosses.[67][68]