ANRV297-EN52-19 ARI 21 November 2006 10:29

Current Status of the

Myriapod Class Diplopoda
(Millipedes): Taxonomic
Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.

Diversity and Phylogeny

Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org

Petra Sierwald1 and Jason E. Bond2

1
Zoology, Insects, Field Museum of Natural History, Chicago, Illinois 60605;
email: psierwald@fieldmuseum.org
2
Department of Biology, Howell Science Complex, East Carolina University,
Greenville, North Carolina 27858; email: bondja@ecu.edu

Annu. Rev. Entomol. 2007. 52:401–20 Key Words

The Annual Review of Entomology is online at
ento.annualreviews.org
This article’s doi:
10.1146/annurev.ento.52.111805.090210
Copyright  c 2007 by Annual Reviews.
All rights reserved
0066-4170/07/0107-0401$20.00
Arthropoda, millipede phylogeny, millipede classification,
millipede fossils, millipede morphology
Abstract
The arthropod class Diplopoda, the millipedes, ranks among the
most diverse groups of terrestrial organisms, with over 12,000
species described. Although they play an important ecological role
in most terrestrial ecosystems, little is known about the group’s di-
versity, morphology, and phylogeny compared with other arthro-
pod groups. We review diplopod natural history and discuss the
historical and current literature pertaining to millipede morphol-
ogy, ecology, chemical defenses, and the paleontological record of
the group’s ancient history. Diplopod systematics, past and present,
are reviewed with a focus on taxonomy, collections, and biogeog-
raphy. The phylogenetics of the class is reviewed, with particular
attention on diplopod placement within the Myriapoda and empha-
sis on recent advances using molecular approaches to phylogenetic
reconstruction. We present (a) the first combined morphological
and molecular analysis of the millipede orders, and (b) a list of criti-
cally evaluated characteristics of nominal clades identifying putative
apomorphies.

401
 ANRV297-EN52-19 ARI 21 November 2006 10:29

INTRODUCTION view provides a brief introduction to milli-

Diplosegment
(diplosomite): body
ring consisting of
two fused somites,
with two leg pairs
and two pairs of
tracheae, makes up
most of the millipede
trunk
BR: body ring
LP: leg pair
Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.
pedes, outlines the current taxonomic status
The millipede class Diplopoda is a mega-
of the group, and presents an overview of mil-
diverse and ancient terrestrial group, with
lipede phylogeny based on a novel total evi-
more than 12,000 nominal species and an
dence analysis.
estimated diversity of approximately 80,000
species (44). Despite their remarkable diver-
sity and importance as detritivores in tem-
DIPLOPOD NATURAL HISTORY
perate and tropical forests (14, 19), ma-
jor problems persist at all taxonomic and Morphology
phylogenetic levels within the group: The
The undisputed diagnostic feature for the
number of described species lags far behind
Diplopoda is the diplosegment condition. A
diversity estimates. There are numerous
millipede body (Figure 1a) consists of the

Collum (neck): monotypic genera; ordinal, subordinal, and

Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org

head and a trunk section with four simple seg-

tergite of legless first familial relationships as well as placement
trunk segment in ments. The remaining body rings (BR) are
of millipedes within the Arthropoda are ei-
pauropods and composed of two segments, each of which
ther unresolved or controversial. Currently,
millipedes carries two leg pairs (LP). The diplosegment
16 orders of extant and 8 orders of ex-
status of the first four segments of the milli-
tinct millipedes are recognized. Taxonomic
pede trunk is still a matter of debate (21, 23,
millipede expertise has always been limited
30, 51, 52). The first trunk segment beyond
to a few researchers, resulting in under-
the head is the legless collum segment, which
representation in collections, especially from
is also found in the Pauropoda, the undis-
the tropics. Most millipede collections har-
puted sister group of the millipedes. Each of
bor large unidentified backlogs (79). This re-
the next three segments carries one pair of
a legs. They originate ventrally and consist of
Head Collum Body rings
seven podomeres (coxa, trochanter, prefemur,
femur, postfemur, tibia, and tarsus). The go-
nads open on or behind the second LP (third
2 3 4 5 6 7 8 trunk ring, progoneate position).
Millipedes have a single pair of antennae
with seven articles (eight in Penicillata) and
four unique sensory cones (diplopod apo-
morphy; see Supplemental Appendix 1, fol-
low the Supplemental Material link from the
Leg pair: 1 2 3 4 5 6 7 8 9 10 11 Annual Reviews home page at http://www.
annualreviews.org) on the last antennomere.
The lateral patches of ocelli, found in most
b c but not all millipede groups, are considered
ocelli compound eye derivatives (83); median eyes
are absent. Several, but not all, millipede
TO orders have a conspicuous organ called the
Antenna Tömösvary organ (TO) (Figure 1b), which
is positioned at the base of the antennae.
Figure 1
The function of the organ is unknown and,
(a) Body organization of a helminthomorph millipede of the orders Julida at least for millipedes, the most recent mor-
and Spirobolida. Appendages at BR7 are modified to gonopods,
sperm-transferring gonopod is solid blue, ozopores indicated. (b) Head of
phological studies of the structure are from
glomerid millipede showing Tömösvary organ (TO). (c) Gnathochilarium 1906 (37). The mouthparts consist of a pair of
(order Julida). mandibles and the plate-like gnathochilarium

402 Sierwald · Bond

 ANRV297-EN52-19 ARI 21 November 2006 10:29
(Figure 1c), the latter interpreted as the fused
first maxilla (36, 48), or as consisting of both
maxillae pairs (53a). Similarities in mandible
structure between centipedes and millipedes
are assumed to be homologous, supporting
myriapod monophyly (24). The gnathochi-
larium consists of several sclerites that vary
among orders, the homology of which is un-
certain (37b, 39). The body end is formed by
the telson, which consists of a preanal ring,
pair of anal valves, and subanal scale. Several
orders possess terminal spinnerets (42). Mil-
lipedes have a rather uniform segmental sys-
Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.
Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org
tem of tracheae (assumed to be homologous
to the tracheal system found in the pauropod
group Hexamerocerata), with either simple or
branched tracheae, each being independent of
the other (89). Members of the largest clade,
the Helminthomorpha, possess a segmental
system of lateral repugnatory glands, with a
single pair at each diplosegment beginning at
BR5 (Figure 1a).
Millipede males of the Helminthomorpha
transfer sperm using modified appendages
(gonopods) on BR7. Gonopods provide the
predominant species-specific characters for
millipede taxonomy. Their functional mor-
phology is poorly known (84), and the ho-
mology of their sclerites with leg podomeres
is uncertain. Males of the other major, albeit
much smaller, clade Pentazonia possess modi-
fied legs at the caudal body end (telopods) that
function in sperm transfer and for clasping the
female. The aflagellate sperm is considered
another apomorphy of the class; sperm mor-
phology is rather complex within millipedes
(5).
Ecology
Hopkin & Read (45) provide a detailed
overview of the ecology of millipedes; we
provide a brief summary here. Most mil-
lipedes are detritivores; their main role in
decomposition is fragmentation of dead plant
material (including wood), thereby stimulat-
ing microbial activity essential for nutrient
cycling (35). In boreal coniferous forests they
may consume up to 36% of the annual conifer
litter (14). Certain species feed on living
plants and can be considered plant pests (6).
Tömösvary organ
Members of the Polyzoniida (Figure 2h,i ) (TO): pair of
and Siphonophorida (Figure 2g) with sensory organs on
strongly modified mouthparts are thought to the head at the base
suck plant juices (especially from roots) and of the antennae,
function unknown
may accumulate alkaloids from these plants in
(also called temporal
their tissue (17). Platydesmida (Figure 2a,b) organ)
may feed on fungi, and Penicillata graze algae
Gnathochilarium:
from bark. Some species are arboreal (e.g., (jaw-lip): plate-like
Zoosphaerium arborealis; 91). Coprophagy is structure formed
essential for weight gain and survival for from fused first
maxilla
some millipedes (60a).
Gonopods:
modified legs of
Predators, Parasites, and Mimicry seventh body ring in
males, used for
Millipedes face assault from numerous preda- sperm transfer (clade
tors and parasites; commensals, especially Helminthomorpha)
mites, are common. Often, mites are associ- Telopods: modified
ated with millipedes; the relationship is likely legs at the caudal
commensal but currently poorly understood. body end, function
Quantitative records of predation on mil- partly in sperm
transfer and clasping
lipedes are sparse and even anecdotal evi-
the female (clade
dence of known predators is rare. The evolu- Pentazonia)
tion of defense secretions and the occurrence
of aposomatic coloration in various groups
with (e.g., the Nearctic Euryuridae; Poly-
desmida) and without defense glands such as
Sphaeromimus (Sphaerotheriida) (92) indicate
the presence of visual predators. A wide range
of animals, such as beetles (81), reptiles, birds,
and various mammals, prey on millipedes in
captivity. Predation by spiders (P. Sierwald,
personal observation), snails (37a), and am-
phibians (e.g., frogs) (17) has also been doc-
umented. Millipedes are hosts to a variety of
parasites; nematodes are likely the most com-
mon (8). Dipterans of the family Phaeomyi-
idae are known parasitoids. Trichomycetes
are obligatory symbiotrophic fungi in mil-
lipede intestines (55, 60, 99), usually oc-
curring in the hindgut. Millipedes are the
intermediate hosts for Macracanthorhynchus
ingens (Acanthocephala) (12), which para-
sitizes raccoons as adults, thus indicating that
raccoons appear to be common predators of
millipedes.
www.annualreviews.org • Millipede Diversity and Phylogeny 403
 ANRV297-EN52-19 ARI 21 November 2006 10:29

Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.
Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org

Figure 2
(a) Platydesmus sp. from Costa Rica (order Platydesmida); (b) Gosodesmus claremontus Chamberlin, 1922
from United States (California) (order Platydesmida); (c) Choctella cumminsi Chamberlin, 1918 from
United States (Tennessee) (order Spirostreptida); (d ) Cambala sp. from United States (North Carolina)
(order Spirostreptida); (e) Falloria apheloriodes Shelley, 1986 from United States (Tennessee) (order
Polydesmida); ( f ) Nacrceus sp. from United States (Virginia) (order Spirobolida); (g) Illacme plenipes Cook
& Loomis, 1928 from United States (California) (order Siphonophorida); (h) Andrognathus corticarius
Cope, 1869 (left) and Brachycybe lecontii Wood, 1864 (right) from United States (North Carolina) (order
Platydesmida); (i ) Petaserpes sp. from United States (Kentucky) (order Polyzoniida). Photos by P. Marek.

Chemical Defenses cretions produced by millipedes, known to

be toxic to insects and vertebrate predators,
Despite their relatively docile appearance,
are of variable composition and span a num-
millipedes can inflict harm on potential preda-
ber of major chemical categories including p-
tors with an array of noxious chemical secre-
benzoquinones, p-cresol, phenols, quinazoli-
tions. With the exception of members of five
nones, alkaloids, terpenoids, and cyanogenic
millipede orders—Polyxenida, Sphaerotheri-
glycosides (2, 26). The small, noncalcareous
ida, Glomeridesmida, Chordeumatida, and
millipedes of the phylogenetically basal or-
Siphoniulida—all millipedes have repugna-
der Polyxenida lack repugnatorial glands but
torial glands and produce chemical secre-
have detachable bristles that entangle preda-
tions when disturbed (2, 25, 45, 61, 71). Eis-
tors (26). Six alkaloid compounds are known
ner and colleagues (25, 27) provide the most
from Glomerida and Polyzoniida species, all
comprehensive reviews of the chemistry of
of which are unique to millipedes (27, 61, 73,
millipede defensive secretions to date. Se-

404 Sierwald · Bond

 ANRV297-EN52-19 ARI 21 November 2006 10:29
98) and cause paralysis in spiders (15). Re-
cent studies have found that polyzoniidans are
preyed upon by dendrobatid poison dart frogs
that then sequester these compounds for their
own defense (17, 72).
The chemical composition of the ben-
zoquinone secretions of the orders Julida,
Spirobolida (Figure 2f ), and Spirostreptida
(Figure 2c,d ) (Juliformia) is perhaps the most
thoroughly documented (2, 4, 22, 27, 62, 64,
74). Studies have confirmed that the odors
produced by these compounds are repulsive
to potential vertebrate predators (63) and are
Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.
Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org
toxic to fungi, nematodes, and bacteria (94).
However, some mammal (e.g., capuchin mon-
keys) and other vertebrate species use milli-
pede secretions to deter mosquitoes (86, 90)
and ticks (16), whereas juliform quinone ex-
cretions actually attract some necrophagous
dung beetle species (74). Polydesmida species
(Figure 2e) produce defensive secretions con-
sisting of mixtures of hydrogen cyanide, ben-
zylaldehyde, phenol, benzoic acid, benzoyl
cyanide, and mandelonitrile (27, 54, 85).
Species in this order typically have bright
aposematic coloration and form putative Mul-
lerian mimicry complexes (27). Despite a
diversity of novel chemical defenses with
proven antimicrobial and insecticidal prop-
erties, much remains to be discovered about
millipede defensive secretions, their chemical
ecology, and potential applications.
Fossil Record
Currently, eight orders of extinct milli-
pedes are recognized: the Microdecempli-
cida, Eoarthropleurida, and Arthropleurida
(placed in the superorder Arthropleuridea by
some authors), the Amynilyspedida (assigned
to the Pentazonia), the superorder Archipoly-
poda with three orders (Cowiedesmida, Eu-
phorberiida, and Archidesmida), and the
Pleurojulida, placed near the Colobognatha
(Figure 3a). The earliest known millipede
fossils, Cowiedesmus eroticopodus Wilson and
Anderson 2004 and Archidesmus macnicoli
Peach 1882, dating from the mid-Silurian
(late Wenlock-early Ludlow, 423–420 Mya)
and Lower Devonian (Lochkovian, 417–412
Mya), respectively, are assigned to the su-
perorder Archipolypoda Scudder 1882 and
placed unequivocally in Helminthomorpha
(95). The Devonian fossils display clear
diplosegments, an apodous collum segment,
anterior trunk segments with single leg pairs,
and modified appendages in proximity to the
eighth ring. These early millipedes are in-
terpreted as fully terrestrial, because of the
inferred presence of a tracheal system (vis-
ible spiracles). Members of the extinct or-
der Euphoberiida Hoffman 1969 are domi-
nant among the rich fossil millipedes of the
Late Carboniferous (Pennsylvanian, 320–290
Mya). Euphoberiids were slightly larger than
modern millipedes and had large eyes with
numerous densely packed ocelli (sometimes
interpreted as compound eyes).
Composition and placement of the su-
perorder Arthropleuridea, containing gigan-
tic members (over 2 m in length) in the
order Arthropleurida Waterlot, 1934 (Early
Carboniferous –Viséan– to Early Permian,
342–271 Mya), smaller forms in the or-
der Eoarthropleurida Shear & Selden, 1995
(Late Silurian to Late Devonian, 422–290
Mya), and tiny members in the Middle
Devonian (398–385 Mya) order Microdecem-
plicida Wilson & Shear, 2000, are controver-
sial. Only recently were the Arthropleuridea
placed within Diplopoda (69, 97). Wilson
& Shear (97) assigned the Microdecempli-
cida to the Arthropleuridea (97), whereas
Kraus & Brauckmann (53) consider them a
sister taxon of the millipede clade Chilog-
natha and placed the remaining two or-
ders of the Arthropleuridea (Arthropleurida
and Eoarthropleurida) as a semiaquatic sis-
ter to the Pselphognatha (Figure 3b) (bristle
millipedes).
Pentazonian millipedes are represented by
the extinct order Amynilyspedida Hoffman,
1969 from the Late Carboniferous, as are
millipedes placed in four extinct spiroboli-
dan families, as well as some members of
the Spirostreptida and Polydesmida. The
www.annualreviews.org • Millipede Diversity and Phylogeny 405
 ANRV297-EN52-19 ARI 21 November 2006 10:29

Pauropoda

Pselaphognatha

Microdecemplicida (Middle Devonian)

Arthropleuridea: Eoarthropleurida (Late Silurian to Late Devonian)
Arthropleurida (Early Carboniferous to Early Permian)

Pentazonia:
Amynilyspedida (Late Carboniferous)
Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.

Cowiedesmida (Mid-Silurian)
Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org

Archipolypoda: Euphoberiida (Late Carboniferous)

Archidesmida (Early Devonian)

Pleurojulida

Colobognatha

Nematophora

Polydesmida

Spirobolida
Juliformia: Julida
Spirostreptida

Pauropoda

Eoarthropleurida
Arthropleuridea:
Arthropleurida

Pselaphognatha

Microdecemplicida

Chilognatha

Figure 3
(a) Cladogram depicting placement of verified millipede fossils (from References 38, 95, and 97).
(b) Placement of the Arthropleuridea (after Reference 53).

406 Sierwald · Bond

 ANRV297-EN52-19 ARI 21 November 2006 10:29
extinct millipede order Pleurojulida Wilson
& Hannibal, 2005 (Pennsylvanian) is con-
sidered a possible sister taxon of Colobog-
natha (96). Permian millipede fossils are
few and not well studied, whereas Meso-
zoic millipedes are usually classified within
the extant orders and families (76). Poly-
xenida, Glomerida, Polyzoniida, Callipodida,
and Chordeumatida are known from Baltic
amber (35–40 Mya), Eocene shales (order Jul-
ida, 54–33 Mya), and Oligocene deposits (33–
23 Mya) (38). Fossils are unknown for the
orders Glomeridesmida, Stemmiulida, Platy-
Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.
Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org
desmida, Siphonophorida, and Siphoniulida.
STATUS OF DIPLOPOD
SYSTEMATICS
Collections
Millipede specimen collections are known
from 268 biological collection institutions lo-
cated in 143 countries (79). Nine major col-
lections house more than 20,000 specimen
series; 77 contain more than 1000 specimen
series (see Table 1). Most millipede collec-
tions are found in North America, with 113
(78 in the United States), and in Europe, with
90 collections (15 in the United Kingdom and
14 in Germany). Australia, South Africa, and
Japan report 14, 7, and 5 collections, respec-
tively. All other areas are underserved with re-
gard to millipedes, especially most of Africa,
Central and South America, and Asia. Spec-
imen collections of the class Diplopoda are
typically housed with other myriapod mate-
rial and are most commonly associated with
the entomological departments of their in-
stitutions. Only a few millipede collections
Table 1 Millipede collections harboring 5000 to over 20,000 specimen series (i.e., lots) (see Reference 79 for
collection acronyms)
Collections
>20,000 lots FSCA, GNM, ITMM, IZCAS, MNHN, NSMT, USNM, VMNH, ZMMU
10,000–20,000 lots AMNH, CAS, FMNH, MFS, MHNG, MRAC, NHMW, SMNG, SMNK, ZMAN, ZMB,
ZMUC
5000–10,000 lots ARPA, BMNH, HNHM, MCZ, MVHN, MZUL, NCSM, NZAC, QVMAG, RMNH, SMF,
ZSMC
are cataloged, some electronically. More than
21,400 type series (including all type cate-
gories) were reported by 89 collections. Many
millipede holdings are historic (i.e., without
current collection growth) and many harbor
large amounts of unsorted backlog.
Taxonomic Diversity and
Distribution
The data presented here are derived from a
worldwide millipede species catalog, which
documents all nominal millipede species and
their bibliographic details in a relational
database. Millipede species names were drawn
from an index card catalog housed in the
Musée National d’Histoire Naturelle (Paris)
and checked against the Zoological Record.
All species records are verified against the
original literature. The millipede species cat-
alog is a work in progress; currently it con-
tains 10,000 verified nominal species records;
species records of the orders Polydesmida and
Julida are not yet complete.
Diplopodologists Past and Present
Linnaeus (56) listed seven species in the
genus Julus. Since 1758 about 200 tax-
onomists have described approximately
12,000 millipede species. The authors Attems
(1868–1952), Chamberlin (1879–1967), and
Verhoeff (1867–1945) each described over
1000 species, followed by Silvestri (1873–
1949), who described 684 species, and Carl
(1877–1944), Loomis (1896–1976), Schubart
(about 1900–1962), Brölemann (1860–1933),
and Pocock (1863–1947) each described
Collection acronyms Total
9
12
12
www.annualreviews.org • Millipede Diversity and Phylogeny 407
 ANRV297-EN52-19 ARI 21 November 2006 10:29
300 to 400 species. Early millipede workers
Koch (1778–1857), Brandt (1802–1879), De
Saussure (1829–1905), Porat (1843–1927),
Karsch (1853–1936), and Cook (1867–1949)
each described between 100 and 200 species.
Diplopod Taxonomy
Higher-level millipede classification appears
to be oversplit; 12,000 described species are
assigned to 2947 genera (4 species per genus
on average) and 145 families (78), with about
68% of all genera being monotypic or con-
Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.
Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org
taining 2 species; 715 generic names are cur-
rently considered synonyms. This indicates
a lack of revisionary work; a vast number of
millipede species are known from their first
description and have never been subjected
to further systematic treatment. In 1860,
100 years after Linnaeus, only 441 millipede
species had been described. The vast majority
of species, almost 7000, were described be-
tween 1890 and 1960, averaging 100 species
per year. The number of species descriptions
per year declined in the second half of the
last century to about 30 per year (1991–2000).
The decline in the annual rate of new species
descriptions is presumably due to a lack of
alpha-taxonomic work and fewer taxonomists;
it is not an indication that species discovery in
millipedes is approaching completeness.
Diversity and Distribution
Estimates of true species diversity (currently
estimated at 80,000 morphological species;
44) are difficult to evaluate. A survey of 35 tax-
onomic monographs published between 1970
and 2004, covering all millipede orders and
all geographic regions, demonstrated that the
fauna of Europe and North America is well-
documented taxonomically (20 studies added
110 new species and synonymized 66 species).
For both regions, comprehensive revisionary
work has been more common. Studies inves-
tigating millipedes from poorly known areas,
such as Africa and South America, resulted
in the description of 262 new species and the
408 Sierwald · Bond
establishment of 124 synonyms of nominal
species.
Conversely, recent molecular studies ad-
dressing species boundaries in a Caribbean
rhinocricid species indicate that population
structuring occurs at a fine geographic scale
and that there is a high potential for cryptic
species, as evidenced by reinforcement where
divergent molecular lineages are sympatric
(10, 11). The cryptic nature of these diver-
gent molecular lineages with respect to geni-
talic (gonopod) differences suggests that tra-
ditional approaches to delineating millipede
species that rely solely upon genitalic and
other morphological characters may underes-
timate true species diversity by at least a factor
of three (10, 11). For many nonvagile inverte-
brate species such as millipedes we are likely
unaware of actual species numbers (9).
Millipede species diversity varies across the
16 orders (see Table 2). As an ancient group,
millipedes inhabited Pangaea (200 Mya) and
as a result occur on every continent except
Antarctica; however, most orders are not dis-
tributed worldwide (Table 2), and distribu-
tion patterns of higher taxa have been at-
tributed to continental drift (40, 45a, 46, 50).
Distribution patterns at the family level show
areas of endemism, for example, the callipo-
didan families Sinocallipodidae and Paracor-
tinidae are restricted to the Yunnan Province
of China, whereas the julidan family Paero-
mopodidae is endemic to North America.
Millipedes are nonvagile. They do not tol-
erate salt water well and cannot fly or bal-
loon (such as spiders) and, as macroinverte-
brates, are less likely to engage in phoresy.
As soil and litter dwellers, millipedes are sus-
ceptible to desiccation (88). As a result, milli-
pede species are often microdistributed, with
closely related species occupying small ranges
in close proximity to each other (58, 91). De-
spite dispersal obstacles, numerous millipedes
are globally invasive, not only thriving around
human settlements, but also successfully col-
onizing disturbed and natural habitats. Al-
most 50% of Britain’s millipede species are
thriving in North America (49), most likely
 ANRV297-EN52-19 ARI 21 November 2006 10:29

Table 2 Biogeography and species diversity of millipede orders

Order Diversitya Distribution
Callipodida 201 North America, Europe, western Asia, southern China, Southeast Asia
Chordeumatida 1237 Worldwide, except for tropical South America and sub-Saharan Africa (present on Madagascar)
Glomerida 271 Northern Hemisphere and Southeast Asia
Glomeridesmida 28 Mexico, northern South America, West Indies, Southeast Asia
Julida 1321 North America to Panama, Europe, Asia north of the Himalayas, Southeast Asia. Mainly
temperate regions
Penicellata 60–70? Worldwide. Dry (not arid) habitats
Platydesmida 69 North and Central America, Europe, Southeast Asia, Japan
Polydesmida 5156 Worldwide
Polyzoniida 127 North America, Caribbean, Europe, southern Africa, Southeast Asia, Indian Ocean Islands,
Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.

New Zealand
Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org

Siphoniulida 2 Currently known only from Mexico and Sumatra

Siphonocryptida 3 Canary and Madeira Islands, Sumatra, Malacca
Siphonophorida 116 North, Central, and South America, Caribbean, South Africa and Southeast Asia, Australia,
New Zealand
Sphaerotheriida 330 Southern Hemisphere: southern Africa and Madagascar, India, Southeast Asia, Australia,
New Zealand
Spirobolida 1248 Western Hemisphere: sub-Saharan Africa, Southeast Asia, Australia. Mainly tropical regions
Spirostreptida 1894 Western Hemisphere: Africa, Asia south of the Himalayas, Australia. Mainly tropical regions
Stemmiulida 124 Tropical South America and Central America, West Indies, central Africa, Sri Lanka and
southern India, New Guinea

a
Indicates the number of nominal species in each order.

through human activities, such as transporta-
tion of nursery stock and soil. The invasive
species Oxidus gracilis (Polydesmida) is also
known as the greenhouse millipede. Other ex-
amples include tramp species such as Rhinotus
purpureus (family Siphonotidae, Polyzoniida)
and Akamptogonus novarae (43). Millipede in-
vasions may go unnoticed because of the gen-
eral lack of alpha-taxonomic discovery and the
lack of ongoing monitoring and survey work
that includes the identification of millipedes
(82).
PHYLOGENY
Diplopod Monophyly, Sister-Group,
and Myriapod Relations
Prior to the Pancrustacea Hypothesis group-
ing Hexapoda with Crustacea, millipedes
were considered a member of the taxon Tra-
cheata Haeckel, 1866 encompassing Arach-
nida and Atelocerata Heymons, 1901 ( =
Hexapoda and Myriapoda). Although milli-
pedes were always grouped with the classes
Symphyla, Pauropoda, and Chilopoda (cen-
tipedes) as Myriapoda, this inclusive taxon
was considered artificial (nonmonophyletic)
by the earliest millipede workers (3). On
the basis of a few key characters, two
schemes of intramyriapod relationships were
proposed.
((Diplopoda, Pauropoda) ((Chilopoda)
(Symphyla, Hexapoda))) invokes the trig-
nath condition of Chilopoda, Symphyla
and Hexapoda as the main character
to separate the dignath Pauropoda and
Diplopoda. The competing scheme was
based on the progoneate/opisthogoneate
condition, classifying myriapods as follows:
(Chilopoda(Hexapoda(Symphyla(Diplopoda,
Pauropoda))). The sister group relationship
between Pauropoda and Diplopoda has rarely
been questioned, supported by morphological

www.annualreviews.org • Millipede Diversity and Phylogeny 409

 ANRV297-EN52-19 ARI 21 November 2006 10:29
characters that include the presence of the
gnathochilarium, the tracheal pouches, and
collum segment in both groups.
Diplopod Placement within the
Arthropoda: Modern Approaches
At present, the class Diplopoda remains un-
equivocally positioned within the group Myr-
iapoda (millipedes, centipedes, symphylans,
and pauropods), the monophyly of which is
supported in most modern phylogenetic stud-
ies (93, 57). However, despite numerous phy-
Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.
Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org
logenetic treatments of the phylum Arthro-
poda and the broader category Ecdysozoa (1,
33), the exact phylogenetic position of myr-
iapods and consequently millipedes remains
equivocal. As summarized by Mallat et al. (57),
there are three competing hypotheses with re-
spect to myriapod placement: sister group to
the Hexapoda (Atelocerata = “Uniramia”),
sister group to the Pancrustacea (Crustacea
+ Hexapoda) forming the clade Mandibu-
lata, and sister group to the Chelicerata form-
ing the clade Paradoxopoda [new name pro-
posed by Mallat et al. (57)]. Recent analyses
using only morphological data (7) and analy-
ses that combine morphological and molecu-
lar data (18S + 28S rDNA; 93) support the
Mandibulata hypothesis. Alternatively, recent
molecular studies of arthropod relationships
employing rDNA sequences (28S + 18S; 57,
65), mitochondrial protein coding genes (34),
and patterns of neurogenesis (47) support the
Paradoxopoda hypothesis.
Relationships within myriapods seem just
as contentious, with no real consensus on
the relative placement of diplopods. Regier
et al. (68) conducted the most recent molec-
ular phylogenetic study of myriapod relation-
ships based on nuclear protein coding genes
(EF-1a, Pol II, and EF-2), uniting diplopods
and chilopods as sister groups, with Symphyla
basal within myriapods followed by Pau-
ropoda. Alternatively, morphological analyses
(7) recover millipedes as the sister group to
pauropods, whereas the combined analyses of
Wheeler et al. (93) recover millipedes as the
410 Sierwald · Bond
sister group to nonchilopod myriapods. Much
work remains to resolve the higher-level rela-
tionships within the Myriapoda.
Historical Development of Diplopod
Classifications
Hoffman (41) gave a detailed account of
the research history of millipedes, mirrored
in the developing and changing classifica-
tion schemes of the class. The Chilognatha
Latreille 1810 were the first recognized clade
within the Diplopoda. Brandt (13) produced
the first detailed classification for the then
known 15 millipede genera, most of which be-
came types of today’s millipede orders, e.g.,
Polyzonium Brandt 1840. Millipede species
discovery and associated progress of its clas-
sification blossomed between 1890 and 1940,
when as many as six highly prolific taxon ex-
perts (Cook, Broelemann, Verhoeff, Attems,
Pocock, and Silvestri) were active. Cook (18)
produced a classification accommodating 50
families and 190 genera, many of the fami-
lies were monotypic at that time, but rapidly
became more diverse as new species were
described. Cook’s classification (with refine-
ments by Silvestri and others) survives to this
day and is employed in Hoffman’s Classifica-
tion of the Diplopoda (41) (Figure 4). Hoffman’s
classification, translated into a phylogenetic
scheme, recognizes few higher clades, result-
ing in a largely unresolved phylogeny for the
Helminthomorpha.
Although millipede orders have remained
stable and their monophyly is assumed (ex-
cept for the position of the spirostreptidan
suborder Cambalidea), many of the orders
appear to be characterized by unique combi-
nations of characters, some of which may be
plesiomorphic, rather than by explicit autapo-
morphies (see Supplemental Appendix 1).
Taxa of higher inclusivity, such as Pentazo-
nia, were proposed on several occasions, but
never universally accepted. However, in the
recent phylogenetic literature (29, 80, 61)
these higher taxa tend to survive rigorous phy-
logenetic analyses.
 ANRV297-EN52-19 ARI 21 November 2006 10:29

Penicillata Polyxenida

Glomerida
Oniscomorpha
Sphaerotheriida
Pentazonia

Limacomorpha Glomeridesmida

Platydesmida
Typhlogena
Siphonophorida
Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.

Ommatophora Polyzoniida
Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org

Siphoniulida

Monocheta Stemmiulida

Helminthomorpha Chordeumatida
Coelocheta
Callipodida

Merocheta Polydesmida

Anocheta Spirobolida
Figure 4

Spirostreptida Classification
employed by
Diplocheta
Hoffman (41), based
Julida on Cook (18).

Diplopod Phylogeny: Current Status der Siphoniulida resulted in a poorly resolved

tree without a monophyletic eugnathan clade.
Higher, ordinal level relationships among the
Phylogenetic analyses of the Diplopoda
diplopod orders remain unresolved. Enghoff
based on an exemplar approach that exam-
(29) presented the first formal cladistic anal-
ines total evidence (e.g., molecular and mor-
ysis of the millipede orders based on mor-
phological characters) are nonexistent. Regier
phological characters using a ground plan ap-
& Shultz (67), and more recently Regier
proach. Major groupings (Figure 5) include a
et al. (68), have attempted the only molecu-
basal Penicillata (order Polyxenida) sister to a
lar phylogenetic analyses that have a broad
grade of lineages, comprising the Pentazonia
enough taxonomic sampling to begin ad-
followed by the Helminthomorpha (compris-
dressing higher-level classification within mil-
ing the clades Colobognatha and Eugnatha).
lipedes. However, conclusions that can be
Ordinal level relationships among the eug-
drawn from these molecular-based phylo-
nathan orders were unresolved. Reexamina-
genies are limited owing to lack of reso-
tion of Enghoff’s character matrix by Sierwald
lution, minimal taxon sampling, and poor
et al. (80) recovered most major clade group-
branch support for deeper nodes within the
ings; however, inclusion of the enigmatic or-

www.annualreviews.org • Millipede Diversity and Phylogeny 411

 ANRV297-EN52-19 ARI 21 November 2006 10:29

Pauropoda

Penicillata

Glomerida
O

Diplopoda
Sphaerotheriida
Pentazonia
L
Glomeridesmida

Platydesmida
Chilognatha
Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.
Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org

Colobognatha Siphonophorida

Polyzoniida
Helminthomorpha

Callipodida
Figure 5
Phylogenetic Chordeumatida
hypothesis of Nematophora
relationships
among the recent Stemmiulida
millipede orders, as
proposed originally
Polydesmida
Eugnatha

by Verhoeff (87),
using today’s clade
labels. Verhoeff Spirobolida
and Attems
employed an older
terminology. Julida
Abbreviations: O, Juliformia
Oniscomorpha; L,
Limacomorpha. Spirostreptida

Diplopoda [note that Regier et al. (68) were a monophyletic lineage, include those orders
primarily interested in myriapod phylogeny]. traditionally placed in the Juliformia and Ne-
In their most recent analysis of the Myri- matophora, which appear as part of an unre-
apoda (68) they examined 28 genera repre- solved polytomy (68).
senting 14 of the 16 extant diplopod orders We present here a novel analysis that
and sampled characters from three nuclear combines a modified version of the morpho-
protein-coding genes (see above). Not sur- logical data matrix presented by Sierwald
prisingly, the analyses recovered a basal Polyx- et al. (80) with the molecular data matrix of
enida, sister to a monophyletic Pentazonia Regier et al. (68). The morphological charac-
and Chilognatha. Within the Chilognatha, ters scored (see Supplemental Appendix 2,
Colobognatha is recovered as a monophyletic follow the Supplemental Material link from
sister group to the Polydesmida. The remain- the Annual Reviews home page at http://
ing Helminthomorpha orders, recovered as www.annualreviews.org) are considered

412 Sierwald · Bond

 ANRV297-EN52-19 ARI 21 November 2006 10:29

Polyxenida
Glomerida 1.0 Cylindroiulus

Glomeridesmida 1.0 Ophyiulus

1.0 Proteroiulus Julida
Sphaerotheriida
1.0 Nemasoma
Siphoniulida
Stemmiulida 1.0 Uroblaniulus
Polydesmida 1.0 Orthoporus
Spirostreptida
Siphonophorida 1.0 Trachyiulus
Siphonocryptida Hiltonius
1.0
Platydesmida 1.0 Narceus Spirobolida
Polyzoniida 0.99
Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.

Orthocricus
Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org

Chordeumatida
1.0 Cleidogona
Callipodida Chordeumatida
1.0 Striaria
Spirostreptida
Abacion Callipodida
Julida 0.96
Spirobolida 0.90 Polyzonium
Polyzoniida
Pauroposia Rhinotus
1.0
0.71 Platydesmus Platydesmida
1.0 Siphonocryptida
0.95
Siphonocybe Siphonophorida
0.98
1.0 Docodesmus
1.0 1.0 Pseudopolydesmus Polydesmida
Oxidus
Stemmiulus Stemmiulida
1.0 Siphoniulida

1.0 Zoosphaerium
Sphaerotheriida
Sphaerotherium
1.0
1.0 1.0 Glomeris Glomerida +
Glomeridesmus Glomeridesmida
Phryssonotus
1.0
Polyxenus Polyxenida
0.89 Plesioproctus
Allopauropus
Eurypauropus

0.01 changes

Figure 6
Phylogenetic hypothesis based on total evidence using Bayesian inference [ln = −17722.60 (harmonic
mean, post burnin)]. The analysis was run for 1 million generations, burnin = 500,000 with an average
standard deviation of split frequencies < 0.006. The Jones model of amino acid substitution had the
greatest contribution to the posterior distribution. Numbers at each node are posterior probabilities.
Ordinal level relationships are summarized on inset tree.

www.annualreviews.org • Millipede Diversity and Phylogeny 413

 ANRV297-EN52-19 ARI 21 November 2006 10:29
homogeneous across each order and thus have
been combined with the generic represen-
tatives used by Regier et al. (68). Orders for
which amino acid sequences were unavailable
(Siphoniulida and Siphonocryptida) were
scored as missing in the molecular partition.
The final concatenated matrix consisted
of 1459 amino acid residues (molecular
data and GenBank accession numbers sum-
marized in Reference 68, table 1) and 41
morphological characters scored for 32 taxa.
Phylogenetic analyses employing Bayesian
inference were conducted with MrBayes
Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.
Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org
Version 3.1.2 (70). We used the “model
jumping” option (aamodelpr = mixed) to
estimate the fixed-rate model for the amino
acid partition; the Mk +  model was used
for the morphological partition. Analyses
consisted of two simultaneous runs, each
with four simultaneous Markov Chain Monte
Carlo (MCMC) chains run initially for 1
million generations. Estimated nuisance
parameters for each molecular partition
were set to be independent. MCMC runs
were summarized and further investigated
for convergence of all parameters using
the sump and sumt commands in MrBayes
and the computer program Tracer Version
3.1 (66). Trees prior to log likelihood sta-
bilization (burnin) and convergence were
discarded before producing a majority rule
consensus tree using the contype = allcompat
command.
The combined Bayesian analysis resulted
in a rather divergent view of diplopod phy-
logeny (Figure 6). Posterior probabilities for
all but two nodes were high—support in the
combined analysis is much higher than pre-
viously shown for independent analyses of
the two partitions, suggesting the presence
of substantial hidden branch support (32).
As in previous analyses, the Polyxenida are
basal, followed by the Pentazonia. Within
the Pentazonia, the Glomerida forms a sis-
ter group with the Glomeridesmida, a lin-
eage not recovered in previous analyses based
on morphology alone. The Helminthomor-
414 Sierwald · Bond
pha are monophyletic with a basal Siphoni-
ulida and Stemmulida. The relatively basal
position of the Stemmulida calls into ques-
tion the monophyly of the Nematophora. The
Colobognatha is recovered as a monophyletic
group but is paired with the Polydesmida,
whereas a monophyletic Juliforma is the sis-
ter group to the Chordeumatida + Callipo-
dida clade. Because the composition of major
clades in the combined analysis departs signif-
icantly from some long-held views regarding
millipede phylogeny (e.g., the Eugnatha), it
presents some difficulties for established char-
acter systems (see character 26 in Reference
80). Although it would be premature to pro-
pose classification changes on the basis of this
analysis, we believe it to be informative be-
cause it demonstrates the equivocal nature and
status of millipede higher-level classification
and exemplifies the challenges faced by future
workers.
CONCLUSIONS
Despite the incredible amount of work un-
dertaken by a few individuals, many issues still
remain largely unresolved in the Diplopoda—
from the placement of millipedes within the
Myriapoda, and the relationships and mono-
phyly of orders, families, and genera, to simply
documenting alpha-taxonomic diversity and
morphological features as well as their im-
pact on soil health and forest ecosystems. Ma-
jor groups, for example the Siphonophorida,
remain terra incognita, with respect to their
morphology. Recent efforts, supported by
funding through the National Science Foun-
dation’s PEET program and the use of mod-
ern technological advances employing dis-
semination via the World Wide Web, how-
ever, generate a significant body of system-
atic infrastructure for the class, such as genus,
species, type, and collection catalogs. In re-
cent studies scanning electron microscopy is
utilized (59, 80, 91, 92). Such improvements
will serve as a catalyst for future diplopod
workers.
 ANRV297-EN52-19 ARI 21 November 2006 10:29

SUMMARY POINTS
1. As macroinvertebrates, millipedes are important decomposers, especially in deciduous
forests. Ecological studies on the role of millipedes are limited.
2. Approximately 12,000 millipede species have been described today; a complete species
catalog is forthcoming.
3. Millipedes are the oldest terrestrial organisms recorded to date.
4. Millipedes are considered monophyletic; pauropods are their undisputed sister group.
5. Most of the 16 extant millipede orders are considered monophyletic (except
Spirostreptida), although unambiguous morphological apomorphies are not yet plen-
tiful. The position of the orders Siphoniulida and Polyzoniida is not yet well estab-
Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.

lished.
Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org

6. The current classification schemes at the subordinal level have not been subjected to
rigorous phylogenetic analyses (with the exception of the order Julida). About 50%
of the 145 millipede families are not identified by putative apomorphies.
7. Entire organ systems are poorly known.
8. Much work on the group’s taxonomy, phylogeny, ecology, morphology, and chemical
defenses remains to be done.

ACKNOWLEDGMENTS
We are grateful to Drs. Richard Hoffman, Sergei Golovatch, and William A. Shear for insightful
discussions about millipede characters. Thomas Wesener, Paul Marek, and Michael Jorgensen
read previous drafts of this manuscript. Drs. Henrik Enghoff and Pavel Stoev shared their
insight into Callipoda characters with us. This work was supported by NSF PEET grants
97-12438 and 05-29715 to Petra Sierwald, William A. Shear, and Jason E. Bond.

LITERATURE CITED
1. Aguinaldo AMA, Turberville JM, Linford LS, Rivera MC, Garey JR, et al. 1997. Evi-
dence for a clade of nematodes, arthropods, and other moulting animals. Nature 387:489–
92
2. Arab A, Zacarin GG, Fontanetti CS, Camargo-Mathias MI, dos Santos MG, Cabrera AC.
2003. Composition of the defensive secretion of the Neotropical millipede Rhinocricus
padergi Verhoeff 1938 (Diplopoda: Spirobolida: Rhinocricidae). Entomotropica 18:79–
82
3. Attems CG. 1926. Myriapoda. In Handbuch der Zoologie 4(1), ed. W Kückenthal,
3. A key overview
T Krumbach, pp. 1–238. Berlin: Walter de Gruyter of all aspects of
4. Attygalle AB, Xu SC, Meinwald J, Eisner T. 1993. Defensive secretion of the millipede diplopod biology
Floridobolus penneri. J. Nat. Prod. 56:1700–6 and systematics.
5. Baccetti B, Burrini AG, Dallai R, Pallini V. 1979. Recent work in myriapod spermatology.
In Myriapod Biology, ed. M Camatini, pp. 97–104. London: Academic
6. Baker AN. 1974. Some aspects of the economic importance of millipedes. Symp. Zool. Soc.
London 32:621–28

www.annualreviews.org • Millipede Diversity and Phylogeny 415

 ANRV297-EN52-19 ARI 21 November 2006 10:29

7. Bitsch C, Bitsch J. 2004. Phylogenetic relationships of basal hexapods among mandibulate

arthropods: a cladistic analysis based on comparative morphological characters. Zool. Scr.
33:511–50
8. Blower JG. 1985. Millipedes. In Synopsis of the British Fauna, ed. DM Kermack, RSK
Barnes. London: Linn. Soc. 242 pp.
9. Bond JE, Beamer DA, Hedin MC, Sierwald P. 2003. Gradual evolution of male genitalia
in a sibling species complex of millipedes. Invertebr. Syst. 17:711–17
10. Bond JE, Sierwald P. 2002. Cryptic speciation in the Anadenobolus excisus millipede species
complex on the island of Jamaica. Evolution 56:1123–35
11. Bond JE, Sierwald P. 2003. Molecular taxonomy of the Anadenobolus excisus (Diplopoda:
Spirobolida, Rhinocricidae) species group on the Caribbean island of Jamaica. Invertebr.
Syst. 17:515–28
12. Bowen RC. 1967. Defense reactions of certain spirobolid millipedes to larval Macracan-
Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.
Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org

thorhynchus ingens. J. Parasitol. 53(5):1092–95

13. Brandt JF. 1840. Remarques générales sur l’ordre des insectes myriapodes. Bull. Sci. Acad.
St. Pétersb. 7:293–328
14. Cárcamo HA, Abe TA, Prescott CE, Holl FB, Chanway CP. 2000. Influence of millipedes
on litter decomposition, N mineralization, and microbial communities in a coastal forest
in British Columbia, Canada. Can. J. For. Res. 30(5):817–26
15. Carrell JE, Eisner T. 1984. Spider sedation induced by the defensive chemicals of milli-
pede prey. Proc. Natl. Acad. Sci. USA 81:806–10
16. Carroll JF, Kramer M, Weldon PJ, Robbins RG. 2005. Anointing chemicals and ec-
toparasites: effects of benzoquinones from millipedes on the lone star tick, Amblyomma
americanum. J. Chem. Ecol. 31:63–75
17. Clark VC, Raxworthy CJ, Rakotomalala V, Sierwald P, Fischer BL. 2005. Convergent
evolution of chemical defense in poison frogs and arthropod prey between Madagascar
and the Neotropics. Proc. Natl. Acad. Sci. USA 102(33):11617–22
18. Cook OF. 1895. Introductory note on the families of Diplopoda. In The Craspedosomatidae
of North America, ed. OF Cook, GN Collins. Ann. NY Acad. Sci. 9:1–7
19. Crawford CS. 1992. Millipedes as model detritivores. Ber. Naturwiss. Med. Ver. Innsbr.
10:277–88
20. Deleted in proof
21. Demange JM. 1967. Recherches sur la segmentation du tronc des chilopodes et des
diplopodes chilognathes (Myriapodes). Mém. Mus. Nat. Hist. Nat. Ser. A 44:188
22. Deml R, Huth A. 2000. Benzoquinones and hydroquinones in defensive secretions of
tropical millipedes. Naturwissenschaften 87:80–82
23. Dohle W. 1974. The segmentation of the germ band of Diplopoda compared with other
classes of arthropods. Symp. Zool. Soc. London 32:143–61
24. Edgecombe GD, Giribet G. 2002. Myriapod phylogeny and the relationships of
Chilopoda. In Biodiversidad, Taxonomı́a y Biogeografia de Artrópodos de México: Hacia una
Sı́ntesis de su Conocimiento, ed. J Llorente Bousquets, JJ Morrone, HP Ulloa, pp. 143–68.
Univ. Nac. Autón. México: Prensas Ciencias
25. Eisner T, Alsop D, Hicks K, Meinwald J. 1978. Defensive secretions of millipedes. In
27. Comprehensive Arthropod Venoms, ed. S. Bettini, pp. 41–72. Berlin: Springer-Verlag
overview of 26. Eisner T, Eisner M, Deyrup M. 1996. Millipede defense: use of detachable bristles to
millipede defenses
entangle ants. Proc. Natl. Acad. Sci. USA 93:10848–51
and chemical
ecology. 27. Eisner T, Eisner M, Siegler M. 2005. Secret Weapons: Defenses of Insects, Spiders,
Scorpions, and Other Many-Legged Creatures. Cambridge, MA: Harvard Univ. Press

416 Sierwald · Bond

 ANRV297-EN52-19 ARI 21 November 2006 10:29

28. Deleted in proof

29. Enghoff H. 1984. Phylogeny of millipedes: a cladistic analysis. Zool. Z. Syst. Evol-
29. First diplopod
forsch. 22(1):8–26 ordinal level
30. Enghoff H, Dohle W, Blower JG. 1993. Anamorphosis in millipedes (Diplopoda): the classification based
present state of knowledge with some developmental and phylogenetic considerations. on rigorous
Zool. J. Linn. Soc. London 109:103–234 phylogenetic
31. Deleted in proof principles.
32. Gatesy J, O’Grady P, Baker RH. 1999. Corroboration among data sets in simultaneous
analysis: hidden support for phylogenetic relationships among higher level Artiodactyl
taxa. Cladistics 15:271–313
33. Giribet G. 2002. Current advances in the phylogenetic reconstruction of metazoan evo-
lution: a new paradigm for the Cambrian explosion. Mol. Phylogenet. Evol. 24:345–57
34. Hassanin A. 2006. Phylogeny of Arthropoda inferred from mitochondrial sequences:
Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.

strategies for limiting the misleading effects of multiple changes in pattern and rates of
Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org

substitution. Mol. Phylogenet. Evol. 38:100–16

35. Hättenschwiler S, Gasser P. 2005. Soil animals alter plant litter diversity effects on de-
composition. Proc. Natl. Acad. Sci. USA 102(5):1519–24
36. Hennig W, Mickoleit G, eds. 1986. Wirbellose II: Gliedertiere. Jena: VEB Gustav Fischer
Verlag. 335 pp.
37. Hennings C. 1906. Das Tömösvaryische Organ der Myriopoden. II. Zeit. Wissen. Zool.
80:576–641
37a. Herbert DG. 2000. Dining on diplopods: remarkable feeding behaviour in chlamyde-
phorid slugs (Mollusca: Gastropoda). J. Zool. 251(1):1–5
37b. Hilken G, Kraus O. 1994. Strucktur und Homologie der Komponenten des Gnathochi-
larium der Chilognatha (Tracheata, Diplopoda). Verh. Nat. Ver. Hambg. 34:33–50
38. Hoffman RL. 1969. Myriapoda, exclusive of Insecta. In Treatise on Invertebrate
38. Comprehensive
Paleontology, Pt. R, Arthropoda 4, ed. RC Moore, 2:R572–606. Lawrence: Geol. classical summary
Soc. Am./Univ. Kans. Press of the diplopod
39. Hoffman RL. 1976. The systematic status of the millipede genus Rajasphaera Attems, fossil record.
1935. Entomol. Mitt. Zool. Mus. Hambg. 5:117–26
40. Hoffman RL. 1978. On the classification and phylogeny of the chelodesmoid Diplopoda.
Abh. Verh. Natwiss. Ver. Hambg. 21/22:129–34
41. Hoffman RL. 1980. Classification of the Diplopoda. Genève: Mus. Hist. Nat. 237 pp.
42. Hoffman RL. 1982. Diplopoda. In Synopsis and Classification of Living Organisms, ed. SP
Parker, pp. 689–724. New York: McGraw Hill
43. Hoffman RL. 1999. Checklist of Millipedes of North and Middle America. Virginia: Mus. Nat.
Hist., Spec. Publ. No. 8. 584 pp.
44. Hoffman RL, Golovatch SI, Adis J, de Morais JW. 2002. Diplopoda. In Arachnida and
Myriapoda, ed. J Adis, pp. 505–33. Sofia-Moscow: Pensoft
45. Hopkin SP, Read HJ. 1992. The Biology of Millipedes. Oxford, UK: Oxford Univ. Press.
233 pp.
45a. Jeekel CAW. 1974. The group taxonomy and geography of the Sphaerotheriida
(Diplopoda). Symp. Zool. Soc. London 32:41–52
46. Jeekel CAW. 1985. The distribution of the Diplocheta and the ‘lost’ continent Pacifica
(Diplopoda). Bijd. Dierkd. 55:100–12
47. Kadner D, Stollewerk A. 2004. Neurogenesis in the chilopod Lithobius forficatus suggests
more similarities to chelicerates than to insects. Dev. Gen. Evol. 214:367–79
48. Kaestner A. 1963. Wirbellose. Lehrbuch der speziellen Zoology, Band 1, 2. Teil: 981–1390.
Jena: VEB Gustav Fischer

www.annualreviews.org • Millipede Diversity and Phylogeny 417

 ANRV297-EN52-19 ARI 21 November 2006 10:29

49. Kime RD. 1990. Spatio-temporal distribution of European millipedes. In Proc. 7th Int.
Congr. Myriapodology, ed. A Minelli, pp. 367–80. Leiden: Brill
50. Kraus O. 1978. Zoogeography and plate tectonics. Abh. Verh. Nat. Ver. Hambg. 21/22:33–
41
51. Kraus O. 1990. On the so-called thoracic segments in Diplopoda. In Proc. 7th Int. Congr.
Myriapodology, ed. A Minelli, pp. 63–68. Leiden: Brill
52. Kraus O. 1998. Phylogenetic relationships between higher taxa of tracheate arthropods.
In Arthropod Relationships, ed. RA Fortey, RH Thomas, Syst. Assoc. Spec. Vol. 55:295–303.
London: Chapman & Hall
53. Kraus O, Brauckmann C. 2003. Fossil giants and surviving dwarfs. Arthropleurida and
Pselaphognatha (Atelocerata, Diplopoda): characters, phylogenetic relationships and con-
struction. Verh. Nat. Ver. Hambg. 40:5–50
53a. Kraus O, Kraus M. 1994. Phylogenetic system of the Tracheata (Mandibulata): on
Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.
Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org

Myriapoda-Insecta interrelationships, phylogenetic age and primary ecological niches.

Verh. Nat. Ver. Hambg. 34:5–31
54. Kuwahara Y, Omura H, Tanabe T. 2002. 2-Nitroethenylbenzenes as natural products in
millipede defense secretions. Naturwissenschaften 89:308–10
55. Lichtwardt RW. 1986. The Trichomycetes: Fungal Associates of Arthropods. New York:
Springer. 343 pp.
56. Linné C. 1758. Systema Naturae per Regna tria naturae, secundum classes, ordines, gen-
era, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima,
reformata., Impensis direct, pp. 1–4. Holmiae, Stockhom: Laurentii Salvii. 824 pp. 10th
ed.
57. Mallat JM, Garey JR, Shultz JW. 2004. Ecdysozoan phylogeny and Bayesian inference:
first use of nearly complete 28S and 18S rRNA gene sequences to classify the arthropods
and their kin. Mol. Phylogenet. Evol. 31:178–91
58. Marek PE, Bond JE. 2006. Phylogenetic systematics of the colorful, cyanide-producing
millipedes of Appalachia (Polydesmida, Xystodesmidae, Apheloriini) using a total evi-
dence Bayesian approach. Mol. Phylogenet. Evol. In press
59. Marek PE, Bond JE. 2006. The rediscovery of Illacme plenipes, the leggiest animal on the
planet. Nature 441:707
60. Margulis L, Jorgensen JZ, Dolan S, Kolchinsky R, Rainey FA, Shyh-Ching L. 1998. The
Arthromitus stage of Bacillus cereus: intestinal symbionts of animals. Proc. Natl. Acad. Sci.
USA 95:1236–41
60a. McBrayer JF. 1973. Exploitation of deciduous leaf litter by Apheloria montana (Diplopoda:
Eurydeamidae). Pedobiologia 13:90–98
61. Meinwald YC, Meinwald J, Eisner T. 1966. 1,2-dialkyl-4(3H)-quinazolinones in the
defensive secretions of a millipede (Glomeris marginata). Science 154:390–91
62. Monro AM, Chada J, Meinwald J, Eisner T. 1962. Defense mechanisms of arthropods.
VI. Para-benzoquinones in the secretions of five species of millipedes. Ann. Entomol. Soc.
Am. 55:261–62
63. Olivieri N, Capone F, Puopolo M, Santucci D, Alleva E. 2001. Response of CD-1 mice
to the chemical defense of a common arthropod. Physiol. Behav. 74:305–11
64. Percy JE, Weatherston J. 1971. Studies of physiologically active arthropod secretions. V.
Histological studies of the defense mechanism of Narceus annularis (Diplopoda: Spirobol-
ida). Can. J. Zool. 49:278–79
65. Pisani D, Poling LL, Lyons-Weiler M, Hedges SB. 2004. The colonization of land by
animals: molecular phylogeny and divergence times among arthropods. BMC Biol. 2:1–10

418 Sierwald · Bond

 ANRV297-EN52-19 ARI 21 November 2006 10:29

66. Rambaut A, Drummond A. 2005. Tracer, a program for analyzing results from Bayesian
MCMC programs such as BEAST & MrBayes. http://evolve.zoo.ox.ac.uk/software.html?
id = tracer
67. Regier JC, Shultz JW. 2001. A phylogenetic analysis of the Myriapoda (Arthro-
poda) using two nuclear protein-encoding genes. Zool. J. Linn. Soc. London 132(4):469–
86
68. Regier JC, Wilson HM, Shultz JW. 2005. Phylogenetic analysis of Myriapoda using
68. First
three nuclear protein-coding genes. Mol. Phylogenet. Evol. 34:147–58 comprehensive
69. Rolfe WDI. 1969. Arthropleurida. In Treatise on Invertebrate Paleontology, Pt. R, Arthropoda treatment of
4, ed. RC Moore, 2:R607–20. Lawrence: Geol. Soc. Am.//Univ. Kans. Press millipede
70. Ronquist F, Huelsenbeck JP. 2003. MRBAYES 3: Bayesian phylogenetic inference under phylogeny using
molecular data.
mixed models. Bioinformatics 19:1572–74
71. Roth LM, Eisner T. 1962. Chemical defenses of Arthropods. Annu. Rev. Entomol. 7:107–
Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.
Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org

36
72. Saporito RA, Donnelly MA, Hoffman RL, Garraffo HM, Daly JW. 2003. A siphonotid
millipede (Rhinotus) as the source of spiropyrrolizidine oximes of dendrobatid frogs. J.
Chem. Ecol. 29:2781–86
73. Schildknecht H, Maschwitz U, Wenneis WF. 1967. Neue Stoffe aus dem Wehrsekret der
Diplopodengattung Glomeris. Naturwissenschaften 54:196–97
74. Schmitt T, Krell FT, Linsenmair KE. 2004. Quinone mixture as attractant for
76. Important
necrophagous dung beetles specialized on dead millipedes. J. Chem. Ecol. 30:731– current update on
40 myriapod fossil
75. Deleted in proof record.
76. Shear WA. 1998. The fossil record and evolution of Myriapoda. In Arthropod Rela-
tionships, ed. RA Fortey, RH Thomas, pp. 211–12. London: Chapman & Hall. 383
78. Most recent
pp. complete listing of
77. Deleted in proof millipede families
78. Shelley RM. 2003. A revised, annotated, family-level classification of the and current
Diplopoda. Arthropoda Sel. 11(3):187–207 classification
scheme.
79. Sierwald P, Reft AJ. 2004. The millipede collections of the world. Fieldiana N.S.
103(1532):1–100
80. Sierwald P, Shear WA, Shelley RM, Bond JE. 2003. Millipede phylogeny revisited 79. First list of the
in the light of the enigmatic order Siphoniulida. J. Zool. Syst. Evol. Res. 41(2):87– world’s diplopod
99 collections, with
81. Snider RM. 1984. Diplopoda as food for Coleoptera. Laboratory experiments. Pedobiologia extensive list of
authors and
26:197–204
deposition of type
82. Snyder B, Draney ML, Sierwald P. 2006. Development of an optimal sampling protocol specimens.
for millipedes (Diplopoda). J. Insect Conserv. 10(3):277–88
83. Spiess T. 1981. Structure and phylogenetic interpretation of diplopod eyes (Diplopoda).
Zoomorphology 98:241–60 80. Most recent
84. Tadler A. 1993. Genitalia fitting, mating behavior and possible hybridization in millipedes reassesment of
of the genus Craspedosoma (Diplopoda, Chordeumatida, Craspedosomatidae). Acta Zool. Diplopoda
phylogeny based on
74(3):215–25
morphological
85. Taira J, Nakamura K, Higa Y. 2003. The identification of secretory compounds from the evidence with first
millipede Oxidus gracilis C.L. Koch (Polydesmida: Paradoxosomatidae) and their variation complete
in different habitats. Appl. Entomol. Zool. 38:401–4 description of the
86. Valderrama X, Robinson JG, Attygalle AB, Eisner T. 2000. Seasonal anointment with order Siphoniulida.
millipedes in a wild primate: a chemical defense against insects? J. Chem. Ecol. 26:2781–90

www.annualreviews.org • Millipede Diversity and Phylogeny 419

 ANRV297-EN52-19 ARI 21 November 2006 10:29

87. Deleted in proof

88. Verhoeff KW. 1928. Klasse Diplopoda I. In HG Bronn’s Klassen und Ordnungen des Tier-
reichs 5. 2. II. Leipzig, Ger.: Akad. Verlag. 1071 pp.
89. Verhoeff KW. 1932. Klasse Diplopoda II. In HG Bronn’s Klassen und Ordnungen
89. Most extensive
overview over all des Tierreichs 5. 2. II. Leipzig, Ger.: Akad. Verlag., pp. 1073–2084
aspects of diplopod 90. Weldon PJ, Adrich JR, Klun JA, Oliver JE, Debboun M. 2003. Benzoquinones from
morphology, millipedes deter mosquitoes and elicit self-anointing in capuchin monkeys (Cebus spp.).
biology and Naturwissenschaften 90:301–4
systematic.
91. Wesener T, Sierwald P. 2005. New giant pill-millipede species from the littoral forest of
Madagascar (Diplopoda, Sphaerotheriida, Zoosphaerium). Zootaxa 1097:1–6
92. Wesener T, Sierwald P. 2005. Revision of the genus Sphaeromimus. Proc. Cal. Acad. Sci.
56(29):557–99
93. Wheeler WC, Giribet G, Edgecombe GD. 2004. Arthropod systematics: the comparative
Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.
Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org

study of genomic, anatomical, and paleontological information. In Assembling the Tree of

Life, ed. J Cracraft, MJ Donoghue, pp. 281–318. New York: Oxford Univ. Press
94. Williams LAD, Singh PDA, Caleb-Williams LS. 1997. Biology and biological action of
the defensive secretion from a Jamaican millipede. Naturwissenschaften 84:143–44
95. Wilson HM, Anderson LI. 2004. Morphology and taxonomy of Paleozoic millipedes
(Diplopoda: Chilognatha: Archipolypoda) from Scotland. J. Paleontol. 78(1):169–84
96. Wilson HM, Hannibal J. 2005. Taxonomy and trunk-ring architecture of pleurojulid
millipedes (Chilognatha: Pleurojulida) from the Pennsylvanian of Europe and North
America. J. Paleontol. 79:1105–19
97. Wilson HM, Shear WA. 2000. Microdecemplicida, a new order of minute arthro-
pleurideans (Arthropoda: Myriapoda) from the Devonian of New York State, USA. Trans.
R. Soc. Edinb. Earth Sci. 90:351–75
98. Wood FW, Hanke JH, Kubo I, Carrol JA, Crews P. 2000. Buzonamine, a new alka-
loid from the defensive secretion of the millipede, Buzonium crassipes. Biochem. Syst. Ecol.
28:305–12
99. Wright KA. 1979. Trichomycetes and oxyuroid nematodes in the millipede, Narceus an-
nularis. Proc. Helminth. Soc. Wash. 46(2):213–23

420 Sierwald · Bond

 Contents ARI 24 October 2006 17:16

Annual Review of

Contents Entomology

Volume 52, 2007

Frontispiece
Charles D. Michener p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p xiv
The Professional Development of an Entomologist
Charles D. Michener p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.

Insect/Mammal Associations: Effects of Cuterebrid Bot Fly Parasites

Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org

on Their Hosts
Frank Slansky p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 17
Phenology of Forest Caterpillars and Their Host Trees:
The Importance of Synchrony
Margriet van Asch and Marcel E. Visser p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 37
Arthropod Pest Management in Organic Crops
Geoff Zehnder, Geoff M. Gurr, Stefan Kühne, Mark R. Wade, Steve D. Wratten,
and Eric Wyss p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 57
The Sublethal Effects of Pesticides on Beneficial Arthropods
Nicolas Desneux, Axel Decourtye, and Jean-Marie Delpuech p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p81
Impact of Extreme Temperatures on Parasitoids in a Climate Change
Perspective
Thierry Hance, Joan van Baaren, Philippe Vernon, and Guy Boivin p p p p p p p p p p p p p p p p p p p p 107
Changing Paradigms in Insect Social Evolution: Insights from
Halictine and Allodapine Bees
Michael P. Schwarz, Miriam H. Richards, and Bryan N. Danforth p p p p p p p p p p p p p p p p p p p p p 127
Evolutionary Biology of Centipedes (Myriapoda: Chilopoda)
Gregory D. Edgecombe and Gonzalo Giribet p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 151
Gene Regulation by Chromatin Structure: Paradigms Established in
Drosophila melanogaster
Sandra R. Schulze and Lori L. Wallrath p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 171
Keys and the Crisis in Taxonomy: Extinction or Reinvention?
David Evans Walter and Shaun Winterton p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 193
Yellow Fever: A Disease that Has Yet to be Conquered
Alan D.T. Barrett and Stephen Higgs p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 209

vii
 Contents ARI 28 September 2006 19:28

Molecular Mechanisms of Metabolic Resistance to Synthetic and

Natural Xenobiotics
Xianchun Li, Mary A. Schuler, and May R. Berenbaum p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 231
Group Decision Making in Nest-Site Selection Among Social Insects
P. Kirk Visscher p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 255
The Role of Allatostatins in Juvenile Hormone Synthesis in Insects and
Crustaceans
Barbara Stay and Stephen S. Tobe p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 277
Nectar and Pollen Feeding by Insect Herbivores and Implications for
Multitrophic Interactions
Felix L. Wäckers, Jörg Romeis, and Paul van Rijn p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 301
Biology and Evolution of Adelgidae
Nathan P. Havill and Robert G. Foottit p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 325
Access provided by Universidade Federal da Paraiba on 05/05/15. For personal use only.
Annu. Rev. Entomol. 2007.52:401-420. Downloaded from www.annualreviews.org

Biology of the Bed Bugs (Cimicidae)

Klaus Reinhardt and Michael T. Siva-Jothy p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 351
The Use of Push-Pull Strategies in Integrated Pest Management
Samantha M. Cook, Zeyaur R. Khan, and John A. Pickett p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 375
Current Status of the Myriapod Class Diplopoda (Millipedes):
Taxonomic Diversity and Phylogeny
Petra Sierwald and Jason E. Bond p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 401
Biodiversity Informatics
Norman F. Johnson p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 421
Cockroach Allergen Biology and Mitigation in the Indoor Environment
J. Chad Gore and Coby Schal p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 439
Insect Conservation: A Synthetic Management Approach
Michael J. Samways p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 465
Interactions Between Mosquito Larvae and Species that Share the
Same Trophic Level
Leon Blaustein and Jonathan M. Chase p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 489

Indexes

Cumulative Index of Contributing Authors, Volumes 43–52 p p p p p p p p p p p p p p p p p p p p p p p p p p p 509

Cumulative Index of Chapter Titles, Volumes 43–52 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 514

Errata

An online log of corrections to Annual Review of Entomology chapters (if any, 1997 to
the present) may be found at http://ento.annualreviews.org/errata.shtml

viii Contents