Diversity, ecology, distribution and biogeography of Diplura

Abstract

Diplura is the sister group to insects and one of the three basal hexapod groups with unique entognathan mouthparts. The order is divided into 10 families, which include 1008 species in 141 genera, with a high proportion of monotypic genera. They are ubiquitous in soils and subsurface terrestrial habitats, as well as have an important role in overall biogeochemical cycles.
We present the first comprehensive review of the global biodiversity and ecology of Diplura. We highlight four aspects of this basal hexapod group: diversity in morphological body plans and sizes; ecology in terrestrial environments from soil to caves; food preference and trophic levels, and their biogeographical and paleobiogeographical significance.
Diplura depends on high humidity and moderate temperatures. They are presumably very sensitive to anthropogenic pressures and climate change, and therefore are a suitable model for ecophysiological studies and evident priority targets for conservation.
We conclude that the future efforts should focus on establishing a molecular phylogeny to clarify the relationships between and within families, as well as to reveal global biogeographical patterns. This will require an increase in sampling effort in several regions of the globe, especially in tropical regions.

Full text

MINOR REVIEW
Diversity, ecology, distribution and biogeography
of Diplura
ALBERTO SENDRA,
1
ALBERTO JIMÉNEZ-VALVERDE,
2
JESÚS SELFA
3
and
ANA SOFIA P. S. REBOLEIRA
4,5
1
Colecciones Entomológicas Torres-Sala, Servei de Patrimoni Històric,
Ajuntament de València, València, Spain,
2
Research Team on Soil Biology and Subterranean Ecosystems, Department of Life Sciences,
Faculty of Science, University of Alcalá (UAH), Madrid, Spain,
3
Laboratori d’Investigació d’Entomologia, Departament de Zoologia,
Universitat de València, València, Spain,
4
Centre for Ecology, Evolution and Environmental Changes (cE3c), and Departamento de
Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon, Portugal and
5
Natural History Museum of Denmark,
University of Copenhagen, Copenhagen, Denmark
Abstract.1. Diplura is the sister group to insects and one of the three basal hexapod
groups with unique entognathan mouthparts. The order is divided into 10 families, which
include 1008 species in 141 genera, with a high proportion of monotypic genera. They
are ubiquitous in soils and subsurface terrestrial habitats, as well as have an important
role in overall biogeochemical cycles.
2. We present the first comprehensive review of the global biodiversity and ecology
of Diplura. We highlight four aspects of this basal hexapod group: diversity in morpho-
logical body plans and sizes; ecology in terrestrial environments from soil to caves; food
preference and trophic levels, and their biogeographical and paleobiogeographical
significance.
3. Diplura depends on high humidity and moderate temperatures. They are presum-
ably very sensitive to anthropogenic pressures and climate change, and therefore are a
suitable model for ecophysiological studies and evident priority targets for conservation.
4. We conclude that the future efforts should focus on establishing a molecular phy-
logeny to clarify the relationships between and within families, as well as to reveal global
biogeographical patterns. This will require an increase in sampling effort in several
regions of the globe, especially in tropical regions.
Key words. Apterygota, basal Hexapoda, cave ecosystems, Entognatha, soil organ-
isms, subterranean biodiversity.
Introduction
Diplurans are one of three entognatous hexapod groups present
in almost every soil, cave or other empty subsurface space. This
order is poorly represented in the scientific literature with only
about 900 publications since Linnaeus wrote the Systema Nat-
urae (1761–1767). In spite of their ubiquity in subsurface terres-
trial habitats, diplurans have been mostly forgotten in ecological
studies and remain without a solid worldwide revision since the
monograph of campodeids by Condé (1956) and the Diplura
checklist by Paclt (1957). A handful of zoologists have devoted
their scientific career to diplurans, beginning with Filippo Silves-
tri (1873–1949) from Italy; from France: Jean Robert Denis
(1893–1969), Bruno Condé, and Jean Pagés (1925–2009); from
Germany: Petr Wygodzinsky (1916–1987); from Czech Repub-
lic Juraj Paclt (1925–2015); from Russia: Boris Pimenovitch
Chevrizov (1951–1993); from USA: Leslie M. Smith
(1903–1976) and Mark Alan Muegge (1956–2015); and finally
from Uruguay: Pablo R. San Martin (1933–1969).
Diplura is considered the sister group to insects and thus the
closest group among the three basal hexapods that include Col-
lembola and Protura (Beutel et al., 2017). Hexapods became ter-
restrial most likely in early Ordovician (Misof et al., 2014),
acquiring breathing capacity through a tracheal system, excre-
tory activity through Malpighian tubules (which are reduced or
absent in some families), and reproduction with indirect sperm
transference by spermatophores (Beutel et al., 2017). The oldest
Correspondence: Ana Sofia P. S. Reboleira, Centre for Ecology, Evo-
lution and Environmental Changes (cE3c), and Departamento de Biolo-
gia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon,
Portugal. E-mail: asreboleira@fc.ul.pt
© 2021 The Authors. Insect Conservation and Diversity published by John Wiley & Sons Ltd on behalf of Royal Entomological Society.
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and
distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
1
Insect Conservation and Diversity (2021) doi: 10.1111/icad.12480

record of a truly dipluran fossil dates back to the Lower Creta-
ceous from Brazil (Wilson & Martill, 2001). However, a
japygid-like doubtful dipluran fossil was described from the
Upper Carboniferous (Kukalová-Peck, 1987). Another four fos-
sil species of campodeids and japygids have been described hith-
erto (Paclt, 1957).
As hexapods, diplurans have an insect-like body plan with
three tagmata: head, thorax, and abdomen. The head has two
frontal antennae with all antennomeres equipped with their
own set of muscles and unique entognathan mouthparts, partially
hidden into two oral folds. The three thoracic segments lack
wings (apterygote hexapods) and have a pair of similar legs end-
ing in a simple tarsus with two claws (pretarsus). The abdomen is
divided into 10 complete segments, some with vestiges of legs
represented by a pair of articulated styli and eversible, water
absorbing vesicles (Weyda, 1976). The last abdominal segment
bears the typical paired cerci, responsible for the common name
two-pronged bristletails or ‘double tails’, that evolved into
a great variety of shapes and function differing among
families (Fig. 1).
Diplurans have successfully colonised hypogean habitats in
soils and in the vast network of caves. They have thrived in all
kind of dark cryptic terrestrial habitats (Racovitza, 1907;
Condé, 1956; Sendra et al., 2020b). Diplurans have a fragile
depigmented cuticle with punctually sclerotized areas at the tip
of the buccal pieces, in the pretarsus and, in some families, in
some distal abdominal segments –including the cerci. Colour
in some diplurans is due to sub-epidermal soluble fats, which
give a few species a yellowish to pinkish colour, or a mix of dif-
ferent patterns as in heterojapygids and some campodeids spe-
cies (Condé, 1956; Paclt, 1956). Diplurans have a vermiform
and flattened body, which gives the group a great mobility and
capability to move along the subterranean network of sometimes
extremely narrow and tiny spaces. To move in these completely
dark environments, the eyeless diplurans possess numerous
kinds of mechanoreceptors and other types of sensorial sensilla,
presumably to detect gradients in humidity, temperature and/or
CO
2
variations. In hypogean environments, diplurans play an
important role in plant litter decomposition and in the generation
of soil microstructure, occupying different trophic levels in the
soil as well as in cave-ecosystems (Condé, 1956). They host bac-
teria, protozoa, fungi, nematodes or other arthropods, and they
feed on a wide range of food sources ranging from fresh or
decomposing plants to dead or alive animals, including microor-
ganisms and fungi (Condé, 1956: Sendra et al., 2020b).
Here we provide a critical review of the order Diplura based
on the current bibliography to highlight four aspects of this basal
hexapod group: diversity in morphological body plans and sizes;
ecology in subsurface environments from soil to caves; food
preference and trophic levels and their biogeographical and
paleobiogeographical relevance.
Diversity
The order Diplura comprises hitherto 1008 species and 88 sub-
species in 141 genera, with a high proportion of monotypic gen-
era (60 genera, 43%) (Figs 1 and 2) (Supporting Information
Table S1). This biodiversity is unequally distributed into 10 fam-
ilies, which exhibit a large variety in body size and shape, behav-
iour, reproduction, and habitat preferences (Denis, 1949;
Koch, 2001; Sendra, 2015). Campodeidae, with 491 species
(49% of dipluran biodiversity), and Japygidae, with 343 species
(34%), account for 83% of all dipluran species. Anajapygidae,
Dinjapygidae, Heterojapygidae, Osctostigmatidae, and Procam-
podeidae represent only 2% of the order’s total biodiversity,
while the remaining three families –Evalljapygidae, Parajapygi-
dae and Projapygidae –contribute up to 15%. Dipluran biodiver-
sity is similar to the other basal hexapod orders, being slightly
higher than in Protura (800 spp.), but lower than in Collembola
(nearly 9000 spp.) (Rusek, 1998; Galli et al., 2019; Potapov
et al., 2020).
Currently, diplurans are divided into three superfamilies,
Campodeoidea, Projapygoidea and Japygoidea, and each has a
well-distinguished body plan (Denis, 1949; Pagés, 1959, 1989;
Koch, 2001; Sendra, 2015). These three taxa show substantial
differences in terminal abdominal cerci, mouthparts, first uros-
ternite, tracheal system, and ovary structure (Denis, 1949;
Pagés, 1959, 1989).
Campodeoidea comprises two families: Procampodeidae and
Campodeidae, both characterised by bearing two long and plur-
iarticulated cerci. The mouthparts include mandibles with a pros-
theca, maxillae without palps, and a labium with a pair of
palpiform processes and an additional pair of spheroidal palps.
The first urosternite bears two subcoxal appendages in lateral
position. In the open tracheal system, spiracles are restricted to
the thorax. Finally, the ovary is simply formed by two sacs sim-
ilar in shape to the testis (Denis, 1949; Pagés, 1959, 1989).
Projapygoidea includes three families: Anajapygidae, Octos-
tigmatidae, and Projapygidae, all of them characterised by bear-
ing two short but pluriarticulated cerci. Each cercus has an apical
orifice, which is the exit of abdominal spinning glands. As to the
mouthparts, like in Campodeoidea the mandibles have a pros-
theca. The maxillae however have palps and internal pectinate
Fig. 1. Overview of Diplura habitus. (a) Campodeidae; (b) Japygidae;
(c) Projapygidae and (d) Heterojapygidae. Scale bars: (a), (b) and
(d) = 10 mm; (c) = 2 mm. [Color figure can be viewed at
wileyonlinelibrary.com]
© 2021 The Authors. Insect Conservation and Diversity published by John Wiley & Sons Ltd on behalf of Royal Entomological
Society., Insect Conservation and Diversity, doi: 10.1111/icad.12480
2 Alberto Sendra et al.

laciniae. The labium has one pair of palpiform processes in addi-
tion to a pair of more or less developed palps. The first uroster-
nite bears lateral styli in addition to two internal subcoxal
appendages. The tracheal system opens with thoracic and
abdominal spiracles. Finally, the ovary is divided into two ovi-
ducts with two ovarioles each (Denis, 1949; Pagés, 1959, 1989).
Japygoidea comprises five families: Japygidae, Evalljapygi-
dae, Parajapygidae, Heterojapygidae, and Dinjapygidae, all of
which bear unarticulated pincer-shaped cerci. At the hind end,
the 8–10 abdominal segments are well sclerotized, bearing the
musculature of the cerci. The mandibles lack a prostheca, and
the maxillae have palps and an internal pectinate lacinia. The tra-
cheal system opens with thoracic and abdominal spiracles.
Finally, the ovary is divided into two oviducts with seven ovari-
oles each (Denis, 1949, Pagés, 1959, 1989).
Below the family level, diplurans display minimal morpho-
logical diversity. Delimitation between species, subgenera, gen-
era, and subfamilies depends mostly on chaetotaxic characters of
large setae (macrosetae), sensilla patterns, modifications in the
glandular and sensorial structures of the first urosternite, and in
some families on the shape and number of teeth in the pincer-like
structurer of the cerci (Silvestri, 1912; Denis, 1930; Pagés, 1953,
1984; Condé, 1956; Smith, 1962). Bareth (1968) suggested the
use of the variability in the shape of spermatozoids fascicles
and spermatophors in Campodeoidea as a taxonomic character.
Recently, scanning electron microscopy studies have provided
Fig. 2. Phylogeny, taxonomical diversity and body length in Diplura compared with Protura and Collembola. Diplura phylogeny adapted from Koch
(2001). [Color figure can be viewed at wileyonlinelibrary.com]
© 2021 The Authors. Insect Conservation and Diversity published by John Wiley & Sons Ltd on behalf of Royal Entomological
Society., Insect Conservation and Diversity, doi: 10.1111/icad.12480
Diplura, a group of basal hexapods 3

additional details about cuticular structures, setae, and sensilla
(Sendra et al., 2019, 2020a). Morphological characters fail to
provide a clear phylogeny below family level and hitherto
molecular data for dipluran species is still very scarce. Conse-
quently, only first advances in molecular analysis, with poor tax-
onomic clarifications, have been produced (Luan et al., 2004; Bu
et al., 2012; Chen et al., 2014).
The body size in diplurans ranges from nearly 1 mm up to
80 mm, a wide variation among soil and cave fauna. Diplurans
are considered from mesofauna to megafauna following the clas-
sification of soil arthropods according to size (Eisenbeis &
Wichard, 1987). Body length in diplurans has a wider range than
in the other basal hexapods whose body length is up to 5 mm in
proturans and 9 mm in springtails (Fig. 2). Procampodeids, ana-
japygids, octostigmatids, and a few parajapygids species are less
than 2 mm long. The body length of most diplurans ranges from
2 mm to 2 cm, and it includes all campodeids, evalljapygids,
projapygids, and the majority of japygids and parajapygids. Only
a few japygids (including most cave-adapted species), dinjapy-
gids, and heterojapygid families exceed a body length of
20 mm (Figs 1 and 2).
Ecology
All diplurans inhabit soil and subsurface terrestrial habitats,
extending from non-consolidated debris in soils to network of
voids in the bedrock, including caves (Condé, 1956; Sendra
et al., 2020b) (Fig. 3).
Diplura, due to their soft body and thin cuticle, depend on high
humidity and moderate temperatures (Condé 1956). Campo-
deids are extremely hydric and have a high transpiration rate,
for example, in Campodea the average loss of water mass is
77.4% h
−1
at 100% relative humidity and 22C (Eisenbeis &
Wichard, 1987). Japygids are considered more thermophilic
and mesic than other diplurans (Eisenbeis & Wichard, 1987)
and have their optimal humidity around 85%, while campodeids
and parajapygids are known to have an optimal fitness under
100% relative humidity (Pagés, 1967b).
Diplurans are well known and mostly diversified in temperate
forests with rich soils, but they are also found under the bark of
tree logs and in mosses (Condé 1956). Coexistence or syntopy
of dipluran species is reported in forest soil habitats, with up to
four different campodeid species found in oak woods in Europe
(Blesi
c, 1987). Dipluran diversity is reduced in boreal forests,
while in tropical forests campodeids are represented mostly by
the Lepidocampinae subfamily in the litter layers, rotten wood
or soil, and in tree epiphytes, while japygids are abundant in deep
soil layers (Delamare Deboutteville, 1950; Condé, 1956). Soils
of scrublands and meadows are occupied by the smallest diplur-
ans such as parajapygids, campodeids or projapygids. Under
stones, it is possible to find the largest diplurans, such as big
japygids, heterojapygids, and dinjapygids. In dry regions, diplur-
ans survive in sites that retain humidity such as temporal water
courses, oasis, or caves (Condé, 1956). Diplurans have also been
collected by chance in ant or termite nests (Silvestri, 1916;
Condé, 1956), as well as in mammal nests (Condé, 1956).
In caves, diplurans from the families Campodeidae and Japy-
gidae are found in karst and in volcanic formations all around the
world, except in extreme cold or dry regions or areas that expe-
rienced these extreme conditions in the past (Sendra
et al., 2020b).
Diplurans can be found along a wide altitudinal range from the
sea level to high mountain areas (Condé, 1956; González, 1964;
Pagés, 1975). Some parajapygids species inhabit the sand or
gravel substratum in intertidal areas (Pagés, 1975; Bu
et al., 2012). To survive in floodable soils, Parajapyx adisi,
which lives in the Central Amazonia forests, builds a cocoon
using the urosternal glands to survive for months (Adis &
Pagés, 2001). Some campodeids have also been found at river
floodplains (Condé, 1960), including temporal water courses
(Sendra et al., 2017) and in the so-called alluvial mesovoid shal-
low substratum (MSS) (Ortuño et al., 2013). At high altitudes,
diplurans can be found in alpine meadows and scree slopes
(Sendra et al., 2017), even when those are seasonally covered
by snow. Almost 50 species have been collected above
2000 m a.s.l., and only a few above 3000 m a.s.l; these high-
altitude species include five campodeids, two japygids, and
two species of the gigantic species of the dinjapygid family:
Dinjapyx barbatus and Dinjapyx michelbacheri in the Andes’
Altiplano (González, 1964). The campodeid Lepidocampa
weberi nepalensis keeps the highest altitude record for the
order; it was collected in Nepal at 4800 m a.s.l. (Condé &
Jacquemin-Nguyen, 1968).
In well-stratified soils, diplurans occupy all soil horizons.
Larger species occupy the upper layers represented by O and
A-horizons and are comprised by the larger campodeids and
japygids, including the giant species of dinjapygids and heteroja-
pygids. Smaller species live in the narrower pores of the B-hori-
zon, where only diplurans with a tiny body (usually under 2 mm
body length and short appendages) can move. Most diplurans are
not actively tunnelling and burrowing soil animals, however,
japygids can build microtunnels in the soil matrix
(Pagés, 1967b), a behaviour that is more evident in heterojapy-
gids (Tillard, 1924). The lower soil layer, the C-horizon
(or MSS) is occupied by soil diplurans. In case of a physical con-
nection of caves with the C horizon, this MSS can be inhabited
by cave-adapted diplurans (Bareth, 1983; Sendra et al., 2017).
The vast cave-ecosystems are found below the soil or under the
rock surface and consist of a network of cracks and voids from
5 mm to hundreds of meters in consolidated rocks (Moldovan
et al., 2018; Culver & Pipan, 2019). These large subterranean
areas are inhabited by a cave-adapted fauna, mostly campodeids
and japygids with larger and slender bodies and appendages than
their soil-adapted relatives (Sendra et al., 2020b).
Very few studies have focused on the abundance of diplurans in
their habitats (e.g. Christian, 1992). The abundance of Diplura
per habitat is far from being known. Drift (1951) found
100 individuals m
−2
of campodeids at the base of old litter in the
humus/mineral soil layer in a beech forest in temperate Europe,
whereas Blesi
c (1987) reported 440–1804 individuals m
−2
in an
oak forest. High specimen density values are also recorded for small
parajapygids living in crops, from 118 individuals m
−2
collected at
5 cm depth in a wheat field in Australia (Greenslade &
Luan, 2018) to 1810–5500 individuals m
−2
at 30 cm depth in a
© 2021 The Authors. Insect Conservation and Diversity published by John Wiley & Sons Ltd on behalf of Royal Entomological
Society., Insect Conservation and Diversity, doi: 10.1111/icad.12480
4 Alberto Sendra et al.

clover field in USA (Macklin, 1956). A behavioural study with japy-
gids estimated 30 specimens of Dipljapyx humberti to be an average
number in a volume of garden soil of 60 ×40 ×50 cm
(Pagés, 1967a). For the other families of Diplura there is no density
data available, but sampling revealed great abundance for evalljapy-
gids, for example, Evalljapyx helferi was described from a single
locality from a redwood humus with 1500 specimens in California,
USA (Smith, 1959); for projapygids, San Martín (1963) quoted
32 specimens under a single stone in Uruguay; and for octostigma-
tids, Rusek (1982) mentioned 51 specimens of Octostigma herbi-
vora in a soil sample from a peanuts plantation in Tonga Islands.
Aggregation behaviour has not been observed in any dipluran
family, while some conspecific avoidance and cannibalism seem
to be common among campodeids (Gunn, 1992). Territorial
Fig. 3. Conceptual model of Diplura habitats, habitus and trophic relationships. [Color figure can be viewed at wileyonlinelibrary.com]
© 2021 The Authors. Insect Conservation and Diversity published by John Wiley & Sons Ltd on behalf of Royal Entomological
Society., Insect Conservation and Diversity, doi: 10.1111/icad.12480
Diplura, a group of basal hexapods 5

behaviour has been suggested for the predatory japygids
(Pagés, 1967a).
Cave-adapted dipluran populations seem to maintain constant
numbers along the year (Sendra & Reboleira, pers. obs.). Diplura
in the MSS show variable seasonal patterns of abundance, that is,
peaking at different seasons in different localities (Eusébio
et al.,, ; Sendra et al., 2017), while soil diplurans show strong
annual variations (Mitrovski-Bogdanovi
c & Blesi
c, 2006; Sen-
dra et al., 2017). This seasonal variation correlates with the
degree of development of the reproductive glands in some cam-
podeid species (Bareth, 1968). Adult females of soil campodeids
lay eggs all year round, except from November to February, dur-
ing a 2-year lifespan (Orelli, 1956). Observational studies of
Campodea lankasteri in a rhizotron showed a higher abundance
from May to mid-September, accounting for approximately 9%
of total soil fauna abundance (Gunn, 1992). Blesi
c (1987)
reported minimal population size of campodeids during the win-
ter in oak forest, similar results were obtained in other sampling
studies (Sendra et al., 2017). In the case of japygids, which have
a lifespan longer than 6 years, Pagés (1963) showed less sea-
sonal variation, perhaps because they survive the annual climatic
variation by reaching deeper layers during periods with extremes
temperatures (Hairston & Byers, 1954; Gyger, 1960).
Pearse (1946) remarked that parajapygids keep regular activity
throughout the year.
While other entognaths, as springtails, have long been used as
model and indicator taxa in soil and ecotoxicology studies
(Smit & Van Gestel, 1998), our knowledge on the effects of con-
taminants in Diplura remains extremely scarce. The effect of sea-
sonal variation in cadmium (Cd) bioaccumulation for Campodea
staphylinus living within litter and with high metal concentration
was studied by Janssen et al. (1990). The study showed a signif-
icant higher Cd concentration in spring and summer compared to
fall and winter seasons, matching the increment in body mass.
The same study pointed out that C.staphylinus showed a higher
Cd bioaccumulation compared to other soil faunal groups, such
as carabid beetles and Mesostigmata mites. The midgut epithe-
lial cells of C.(Monocampa)devoniensis were microanalysed
and their electron-dense granules were found to be strongly
influenced by the environmental bioavailability of metals with
the capacity to bioaccumulate Fe, Mn, Zn, Pb, and Cu (Pigino
et al., 2005). Another study on the effects of increasing soil metal
contamination on arthropod communities suggests that Diplura
(together with the other entognaths orders) may tolerate high
concentrations of Pb and Sb in soils (Migliorini et al., 2004).
Diplurans have also been reported to be influenced by soil acid-
ity (Paoletti et al., 1996). The potential of Diplura as relevant
taxa for evaluating anthropogenic disturbance in soils has been
highlighted because they are well represented in all kinds of soil
and subsurface habitats and are impacted by environmental
changes (Blasi et al., 2013).
Food preference and trophic levels
Overall, diplurans play multiple roles in soil food webs –from
primary consumers of root plants and detritivores, to secondary
and tertiary consumers, and they can even be top invertebrate
predators. Their feeding preferences vary across families and
are related to size, shape of mandibular and maxillar structures,
and to the type of terminal cerci (Christian & Bauer, 2005). Cam-
podeids (up to 10 mm body length) have long, fragile, multiarti-
cular cerci and mouthparts with grasping and crushing function.
They are omnivores with a generalist diet, eating from fresh
roots, fungal hyphae and spores to decay organic matter or even
tiny invertebrates, so they can be considered either decomposers
or primary and secondary consumers (Bareth, 1986;
Gunn, 1992; Blesi
c, 1999; Christian & Bauer, 2005). Japygoidea
(up to 6 cm body length) have unsegmented pincer-shaped cerci,
heavily sclerotized and muscled, with offensive and defensive
roles, and mouthparts optimised for perforating and tearing.
Thus, they are mostly predators feeding on small arthropods
such as mites, springtails, symphylans, insect larvae and others
diplurans, and very rarely feed on terrestrial isopods, but they
are also known to feed on organic debris and fungal mycelia
and spores (Christian & Bauer, 2005). Within Japygoidea, japy-
gids are predators while heterojapygids and dinjapygids are top
invertebrate predators, thus representing the highest level of the
trophic pyramid for all invertebrates. For instance, in the Andes,
dinjapygids have been reported to apparently exclude scorpions
and occupy their ecological ‘niche’(González, 1964). Parajapy-
gid species feed on plant roots including crops (Reddell, 1985);
evalljapygids probably also mostly feed on plants since no ani-
mal remains have been found in the guts of many species
(Smith, 1959), with the exception of one Evalljapyx macswaini
specimen that had insect parts in its gut, probably thrips
(Smith, 1960). Finally, Projapygoidea (2 mm) have short
multi-articulated glandular cerci with a defensive and offensive
function, showing a mixed feeding behaviour by predating on
microarthropods such as mites and tiny pseudoscorpions (San
Martín, 1963) but also consuming plant roots (Rusek, 1982).
Diplurans are predated by several arthropod groups. Larger
diplurans feed on smaller diplurans and at the same time are
known to be predated by centipedes and ground beetles
(Kasaroff, 1935; Gunn, 1992).
Symbiotic interactions surrounding diplurans, most of the
time with unclear dependence degrees, comprise a wide range
of organisms including bacteria, hyphae and spores of fungi,
‘Amphoromoph’fungi, Gregarinia cysts, larvae of Gordiidae
nematomorphs, and nematode larvae or Acari (Paclt, 1957;
Bareth, 1974).
Distribution and biogeography
The order Diplura is an ideal model for biogeographical studies;
diplurans are wingless hexapods with limited dispersal capaci-
ties and with little tolerance to temperature variations and dry-
ness. Besides, many species live confined in underground
habitats, and the taxon has its ancient origin in the Early Ordovi-
cian, reflected in a Pangean distribution for the most species-rich
families (i.e., Campodeidae and Japygidae) and more limited
distribution ranges for the rest of the families (Tables 1 and 2).
Nevertheless, some ecological traits can complicate the under-
standing of their biogeographical patterns. For example, some
campodeids and parajapygids can survive in temporal interstitial
© 2021 The Authors. Insect Conservation and Diversity published by John Wiley & Sons Ltd on behalf of Royal Entomological
Society., Insect Conservation and Diversity, doi: 10.1111/icad.12480
6 Alberto Sendra et al.

flooded habitats for long periods (Condé, 1960), and parajapy-
gids can produce resistant cocoons (Adis & Pagés, 2001) that
can be easily dispersed. Some species are considered invasive,
such as Campodea (Monocampa)devoniensis, native to Western
Europe but found in urban gardens and city surroundings around
the world, as well as in certain Darwinian islands (those never
connected to mainland) such as Saint-Helena or the Canaries
(Paclt, 1966; Condé & Bareth, 1970). The lack of an internal
phylogeny (Sendra et al., 2020b), and the large geographical
sampling bias (54% of all known Diplura records are located in
France, Italy, Spain and USA), are currently the two major limi-
tations to understand the biogeographical history of the taxon.
Diplurans have been found in all continents, except in Antarc-
tica, since they never managed to overpass the Polar circles. This
vast distribution is somewhat smaller compared to the two other
basal hexapod groups, where Protura slightly overpass the Arctic
Circle (Galli & Rellini, 2020) and Collembola even managed to
colonise Antarctica (
Avila-Jiménez & Coulson, 2011). Among
diplurans, only campodeids have been found living in northern
latitudes. For instance, Campodea (C.) fragilis was recorded
from Vega Island, Norway (Lie-Pettersen, 1907), located at
65N, slightly South of the Arctic Circle, and two other campo-
deids, Metriocampa allocerca and Metriocampa rileyi, were
found at 64N and 56N in Alaska, respectively (Sikes &
Allen, 2016). At the lowest southern latitudes there is again
another a campodeid, Campodea (Campodea)lahillei, which
was found at 49S in the Santa Cruz province, Argentina
(Silvestri, 1931). Japygids and Evalljapygids species are
restricted to warmer areas although two species, Dipljapyx hum-
berti and Metajapyx leruthi, have been found at 50N in Belgium
(Silvestri, 1948), and Evalljapyx saundersi was located at 49N
in Vancouver Island, Canada (Saunders, 1946; Pagés, 1996).
Regardless of the aforementioned limitations, the existing
data (1008 described species sampled, Supporting Information
Table S1, from more than 7000 localities around the world) per-
mit to delimit distribution patterns, as well as to arrive at some
paleobiogeographical conclusions. For instance, the biogeo-
graphical distribution of diplurans follows the general patterns
described by Darlington (1957) and Vigna Taglianti
et al. (1992, 1999). According to that criteria, Diplura fall into
the W-Palearctic, containing the distribution areas of 35% of
all diplurans and 43% of all dipluran genera. In the whole
Holarctic, the percentages rise to 56% of the species and 90%
of the genera. Surely, such high numbers may be influenced by
the biased sampling and lack of taxonomical studies in other
regions.
At the family level (Table 1), the Holarctic region is charac-
terised by the high diversity of campodeids (336 out of the
491 species) and by two highly diverse genera, the cosmopolitan
Campodea (143 out of the 180 species) and the endemic Plusio-
campa (70 species), as well as a good representation of japygids
(139 out of the 340 species). In addition, the Palearctic region is
characterised by its endemic and small procampodeid family
(2 species). In the Ethiopian and Neotropical regions, three fam-
ilies are noteworthy because of their diversity: japygids (126 out
of the 340 species), parajapygids (37 out of the 62 species), and
projapygids (36 out of the 42 species). The Oriental region
shows a high diversity of japygids (58 out of the 340 species)
(Table 1). The five species of the anajapygid family are distrib-
uted in the Holarctic (3 species.), Oriental (1 sp.), and Neotropi-
cal (1 species) regions (Table 1). The rest of the families, all with
a very low number of species, have more restrictive distribution
ranges. Two of the three octostigmatid species live in the Orien-
tal region and one in the western Australian island. The 10 het-
erojapygids occupy the Eastern Palearctic (five species) and
Australian (five species) regions. And finally, the five species
of dinjapygids live exclusively in east territories of the Neotrop-
ical region (Table 1).
The current distribution of Diplura is linked to the fragmenta-
tion of Pangea and drift during the Mesozoic and Cenozoic era
(Table 2). As mentioned above, not only campodeids and japy-
gids but also parajapygids show a Pangean distribution, which
is a distribution that can also be inferred in some monophyletic
lines such as the tachycampoids (Bareth & Condé, 1981; Sendra
et al., 2020a, 2020b). For the Campodeidae family, Laurasia was
probably their centre of diversity judging from the high number
of species and genera (381 out of the 491 species and 41 out of
the 58 genera) found in Eurasia and North America, which
include some shared taxa such as Campodea s. str., Litocampa,
Podocampa and Metriocampa. Some campodeids genera and
subgenera have a Gondwana distribution, and they are found in
most of its remains landmasses, for example, Notocampa
(New Zealand, Australia, Madagascar, Africa and South-Amer-
ica), Lepidocampa (Australia, India, Madagascar, Africa and
Table 1. Number of Diplura species and genera (between brackets) per family by biogeographical regions.
E-Palearctic W-Palearctic Nearctic Australian Oriental Ethiopian Neotropical Holarctic World
Campodeidae 30 (12) 246 (19) 92 (16) 20 (8) 20 (8) 47 (14) 45 (13) 366 (38) 491 (58)
Procampodeidae 1 (1) 1 (1) 2 (1) 2 (1)
Projapygidae 4 (2) 1 (1) 2 (1) 8 (2) 28 (4) 4 (2) 42 (4)
Anajapygidae 1 (1) 2 (2) 1 (1) 1 (1) 3 (2) 5 (2)
Octostigmatidae 1 (1) 2 (1) 3 (1)
Japygidae 18 (7) 89 (17) 32 (7) 20 (5) 58 (13) 63 (17) 63 (13) 139 (27) 340 (61)
Parajapygidae 3 (1) 9 (1) 5 (2) 4 (1) 8 (1) 20 (2) 17 (2) 15 (2) 62 (4)
Evalljapygidae 26 (3) 22 (3) 26 (3) 47 (5)
Dinjapygidae 6 (1) 6 (1)
Heterojapygidae 5 (4) 5 (1) 5 (4) 10 (4)
Total taxa by region 56 (24) 350 (41) 158 (31) 51 (17) 91 (25) 139 (36) 181 (36) 560 (79) 1008 (141)
© 2021 The Authors. Insect Conservation and Diversity published by John Wiley & Sons Ltd on behalf of Royal Entomological
Society., Insect Conservation and Diversity, doi: 10.1111/icad.12480
Diplura, a group of basal hexapods 7

South-America), and Campodella (Australia, Madagascar and
Africa). In addition to these genera, Campodea (Indocampa)is
restricted to landmasses from East-Gondwana (Australia, India,
and Madagascar), whereas Natalocampa is restricted to South-
America and South-Africa (West-Gondwana). The diversity
centre for japygids is uncertain; today’s Laurasia territory has
173 species and 35 genera, meanwhile today’s Gondwana holds
168 species and the same number of genera. Some japygid gen-
era, such as Metajapyx and Occasjapyx, are good examples of
the connection between the Laurasian plates and their split in
the Early Cenozoic. Several japygid genera are shared between
Gondwana plates, such as Mesjapyx (Australia, India, Madagas-
car, and Africa), Indjapyx (Australia and India), and Austrjapyx,
Hapljapyx and Teljapyx (Africa and South-America). In the case
of the projapygids, the massive diversity in the Gondwana terri-
tory, with 41 out of the 42 species (39 species mostly in Western
Gondwana, today’s Africa and South-America) indicates its
probable centre of origin in the Early Cretaceous before the
opening of the South Atlantic. In parajapygids, the existence of
a hot diverse centre is Africa with 27 out of the 62 species, fol-
lowed by Eurasia with 13 species and South-America with
12, makes it difficult to decide on its probable centre of origin.
Furthermore, parajapygids can live in the marine coast and flu-
vial sediments, giving them a certain capacity for long distance
dispersal and to colonise new regions. This can explain the pres-
ence of Parajapyx isabellae in all continents (Greenslade &
Luan, 2018). The distribution range of evalljapygids reaches
from the western regions of North America (34 out of the 47 spe-
cies) throughout South America (12 species). The dinjapygids,
with six species, are distributed in the western South America,
and their proposed close phylogenetic relationship with the Het-
erojapygidae (with 10 species in Australia, New Zealand, and
Eurasia) probably implies a wider Pangean distribution of the
common ancestor (Markus Koch, pers. comm.). The remaining
dipluran families: procampodeid, anajapygid, and octostigmati-
did, have a handful of species, making it impossible to suggest
any centre of origin, but their relationship with the other families
suggests, at least, a Laurasian and Gondwanan origin for
procampodeids and anajapygids, respectively (Table 2).
Final remarks and future perspectives
In summary, as this review has shown, Diplura is an important
and abundant group, both in soils and cave ecosystems, occupy-
ing a variety of trophic levels. With their ancient origin, Diplura
is a crucial taxon to understand the early phase of insect evolu-
tion, the most diverse group of animals on Earth. Diplura is also
an impressively diverse group with an astonishing variety of
shapes and morphologic body plans, including unique sensorial
and glandular structures. Nevertheless, diplurans have attracted
scarce attention from zoologists, and as a result the knowledge
is often restricted to taxonomy and geographically biased. Future
efforts in the study of the order Diplura should focus on:
•Establishing a molecular phylogeny to clarify the relation-
ships between and within families, as well as the
biogeographical and paleaobiogeographical patterns;
Table 2. Number of Diplura species and genera (between brackets) per family in the different Pangea tectonic plates.
Eurasia
North-
America Laurasian New Zealand Australia India Madagascar Africa
South-
America Gondwana E-Gondwana W-Gondwana
Campodeidae 280(31) 104(18) 381 (40) 1 (1) 19 (8) 4 (2) 13 (4) 49 (18) 35 (13) 113 (27) 31 (8) 83 (24)
Procampodeidae 1 (1) 1 (1) 2 (1) 1 (1) 1 (1) 1 (1)
Projapygidae 1 (1) 1 (1) 1 (1) 1 (1) 11 (2) 29 (4) 41 (4) 2 (1) 39 (4)
Anajapygidae 2 (2) 2 (2) 1 (1) 2 (1) 3 (1) 1 (1) 2 (1)
Octistigmatidae 2 (1) 2 (1) 1 (1) 1 (1) 1 (1)
Japygidae 136 (31) 35 (7) 171 (35) 2 (1) 17 (4) 23 (4) 1 (1) 66 (20) 60 (14) 168 (35) 42 (8) 126 (30)
Parajapygidae 13 (1) 8 (3) 20 (3) 4 (1) 1 (1) 27 (2) 12 (1) 42 (2) 4 (1) 38 (2)
Evalljapygidae 34 (4) 34 (4) 12 (2) 12 (2) 12 (2)
Dinjapygidae 6 (1) 6 (1) 6 (1)
Heterojapygidae 5 (4) 5 (4) 1 (1) 4 (1) 5 (1) 5 (1)
Total taxa by plate 438 (70) 184 (35) 618 (91) 4 (3) 46 (16) 30 (9) 14 (5) 156 (44) 154 (35) 402 (75) 86 (21) 307 (65)
© 2021 The Authors. Insect Conservation and Diversity published by John Wiley & Sons Ltd on behalf of Royal Entomological
Society., Insect Conservation and Diversity, doi: 10.1111/icad.12480
8 Alberto Sendra et al.

•Increasing the sampling effort in several regions of the globe,
especially in the tropical regions;
•Including Diplura into soil and cave ecological studies,
reflecting their importance in both ecosystems;
•Generating ecotoxicological information to understand the
ecophysiological tolerance of Diplura;
•Exploring their potential to serve as indicator species in
global change studies, as expected looking at their narrow
hydric and thermal tolerance.
Despite of poorly known, the ubiquity of Diplura in terrestrial
ecosystems, paired with their sensitivity to environmental
change, makes them important target key species for conserva-
tion, which should not be neglected in environmental
assessment.
Acknowledgements
We would like to thank Loris Galli, who inspired us with his
studies on Protura, to Nikolaus Szucsich and L’ubomír Ková
c
for their careful review, to Teresa Molina Jiménez and Ricardo
Gimémez Mezquita for support in producing Figs 2 and 3, to
Lucia Maltez for the English revision, to Louis Deharveng for
the Projapygidae image in the Fig 1c, and to Yunxia Luan for
the Heterojapygidae photo in Fig. 1d. AJ-V was supported by
the Spanish Ramón y Cajal Program (RYC-2013-14441), which
is financed by the Spanish Ministry of Science, Innovation and
Universities. ASPSR is funded by a research grant (15471) from
the VILLUM FONDEN.
Data availability statement
Data are available in the cited references.
Supporting information
Additional supporting information may be found online in the
Supporting Information section at the end of the article.
Table S1 Species and subspecies of the order Diplura.
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Accepted 10 February 2021
Editor: Raphael Didham; Associate Editor: Thomas Bolger
© 2021 The Authors. Insect Conservation and Diversity published by John Wiley & Sons Ltd on behalf of Royal Entomological
Society., Insect Conservation and Diversity, doi: 10.1111/icad.12480
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