#ZooKeys

ZooKeys 1180: 51-65 (2023)
DOI: 10.3897/zookeys.1180.109099

Research Article

The first record of the genus Julolaelaps Berlese (Acari,
Mesostigmata, Laelapidae) in Republic of Korea and description
of a new species on a captive giant African millipede
(Spirostreptidae, Archispirostreptus)

Omid Joharchi'?®, Seoyoung Keum?®, Chuleui Jung'“®

1 Agriculture Science and Technology Institute, Andong National University, Andong, Republic of Korea
2 Institute of Environmental and Agricultural Biology (X-BIO), Tyumen State University, Tyumen, Russia
3 Silkworm and Insect Management Center, Sangju, Republic of Korea

4 Department of Plant medicals, Andong National University, Andong, Republic of Korea
Corresponding author: Chuleui Jung (cjung@andong.ac.kr)

OPEN Qaccess

Academic editor: Farid Faraji
Received: 6 July 2023
Accepted: 29 August 2023
Published: 15 September 2023

ZooBank: https://zoobank.
org/711DA3A4-B9AC-49F8-AAA4-
0682823DED14

Citation: Joharchi 0, Keum S, Jung
C (2023) The first record of the
genus Julolaelaps Berlese (Acari,
Mesostigmata, Laelapidae) in
Republic of Korea and description
of a new species on a Captive giant
African millipede (Spirostreptidae,
Archispirostreptus). ZooKeys 1180:
51-65. https://doi.org/10.3897/
zookeys.1180.109099

Copyright: © Omid Joharchi et al.

This is an open access article distributed under

terms of the Creative Commons Attribution
License (Attribution 4.0 International -
CC BY 4.0).

Abstract

This paper reports on a new species of mite of the genus Julolaelaps Berlese in Re-
public of Korea. Females and males of a new species, Julolaelaps gigas sp. nov., were
collected on a captive giant African millipede, Archispirostreptus gigas (Spirostreptida:
Spirostreptidae). The new species is described and illustrated based on morphological
characters of the adult females and males and compared with known congeners. This
new species is the first record of Julolaelaps from Republic of Korea. In addition, an
updated key to all known species of the genus is presented.

Key words: Arthropod-associated mites, Dermanyssoidea, East Palaearctic region,
Gamasina, Indomalayan Realm, mesostigmatic mites, Parasitiformes, Spirostreptidae,
taxonomy

Introduction

Like most other arthropod groups, millipedes have attracted a mite fauna. The
mites associated with millipedes are taxonomically and ecologically diverse,
and about eighteen mite families have been recorded from the two orders Me-
sostigmata and Sarcoptiformes (Farfan and Klompen 2012).

Depending on the millipede and mite species, the nature of the symbiotic rela-
tionship can range from commensalism to obligate parasitism (Gerdeman et al.
2000; Farfan and Kliompen 2012). Some of these mites may benefit their millipede
hosts by helping to control populations of Acaridae, which sometimes become
pests of captive millipedes (Swafford and Bond 2010; Farfan and Klompen 2012).

Ecological relationships such as these, with varying degrees of intimacy in
the relationship between host animals and their associated mites, may rep-
resent a series of evolutionary stages from phoresy to parasitism. The ge-
nus Julolaelaps Berlese is one of the groups of Mesostigmata that includes

51

Omid Joharchi et al.: The genus Julolaelaps Berlese in Republic of Korea

22 nominal species commonly associated with millipedes, mainly in Juliformia
(Diplopoda) (Moraes et al. 2022), but some described species are associated
with hosts in Polydesmida (Diplopoda) (Ishikawa 1986) and one species occa-
sionally from the soil (Nemati et al. 2015). The genus is geographically distrib-
uted in Africa, the Middle East, East, South and Southeast Asia (Berlese 1916;
Maes 1983; Fain 1987; Kontschan 2005; Uppstrom and Klompen 2005; Sal-
mane and Telnov 2007; Moraza and Kazemi 2012; Nemati et al. 2015; Moraes
et al. 2022). However, the nature of their symbiotic relationship (mutualism,
commensalism and parasitism) with millipedes has not yet been confirmed
(Salmane and Telnov 2007).

Julolaelaps was first established by Berlese (1916) for a small group of
mites living on julids (Juliformes) belonging to the family Iphiopsididae. It was
subsequently included in the Laelapidae-Hypoaspidinae by Vitzthum (1942:
763) and in the Laelapidae-Iphiopsidinae by Moraza and Kazemi (2012: 12). In
this study, we follow Maes (1983) and Moraza and Kazemi (2012) in keeping
the Julolaelaps as a separate genus of the family Laelapidae Canestrini, 1891,
subfamily Iphiopsidinae Kramer, 1886.

Several authors have already recorded a collection of Laelapidae associated
with insects and soil from the Republic of Korea (Kontschan et al. 2015, 2016;
Keum et al. 2016, 2017; Joharchi et al. 2018, 2019; Oh et al. 2023). The present
paper is part of a project that aims to increase the knowledge of the mite fauna
of the Republic of Korea, particularly the poorly studied fauna of insect-asso-
ciated species of mesostigmatic mites. Towards this aim, we herein describe
a new species belonging to the genus Julolaelaps on the basis of female and
male specimens collected on captive giant African millipede, Archispirostrep-
tus gigas (Peters) (Spirostreptida: Spirostreptidae) in Republic of Korea. In ad-
dition, an update of the key of Julolaelaps species is presented to include the
new species.

Materials and methods

The millipbedes were purchased for exhibition purposes and kept in a plastic
cage with a sufficient amount of corroded oak sawdust. Mites were removed
from the captive giant African millipede using a fine brush, cleared in lactic acid
solution and mounted in PVA medium (Downs 1943). The line drawings and
examinations of the specimens were performed with a Zeiss Axio Imager A2
compound microscope equipped with differential interference contrast optical
systems and an attached Axiocam 506 color camera (Carl Zeiss, Germany).
Most images were captured in stacks (with focal depth manually controlled).
Selected images were combined using Helicon Focus 7.6.4 Pro (Helicon Soft
Ltd, 2000). Digital drawings were prepared using Adobe Photoshop CS2 soft-
ware based on the original pencil line drawings. Images and morphological
measurements were taken via ZEN 2012 software (version 8.0). Measurements
of structures are expressed as ranges (minimum-—maximum) in micrometres
(um). The length and width of the dorsal shield were taken from the anteri-
or to the posterior margins along the midline, and at level of r4, respectively.
Length and width of the sternal shield were measured at the maximum length
and broadest points, respectively. The length of the epigynal shield was mea-
sured along the midline from the anterior margin of the hyaline extension to the

ZooKeys 1180: 51-65 (2023), DOI: 10.3897/zookeys.1180.109099 52

Omid Joharchi et al.: The genus Ju/olaelaps Berlese in Republic of Korea

posterior margin of the shield, and its maximal widthwas measured posterior
to genital setae st5. Leg length was measured from the base of the coxa to the
apex of the tarsus (excluding the pre-tarsus). The nomenclature used for the
dorsal idiosomal chaetotaxy follows that of Lindquist and Evans (1965), the
notations for leg and palp setae follow those of Evans (1963a, b), and other an-
atomical structures mostly follow Evans and Till (1979). Notations for idioso-
mal pore-like structures (gland pores and poroids/lyrifissures) and peritrematal
shield follow mostly Athias-Henriot (1971, 1975). The notations for pore-like
structures on the sternal shield and for the peritrematal shield region also fol-
low modifications and additions by Johnston and Moraza (1991). Holotype and
paratypes of the new species were deposited at the National Institute of Biolog-
ical Resources (NIBR), Republic of Korea.

Results

Genus Julolaelaps Berlese

Julolaelaps Berlese, 1916: 31. Type species Julolaelaps dispar Berlese, 1916,
by original designation.
Hypoaspis (Julolaelaps). — Ryke, 1959: 7.

Remarks. The concept of Julolaelaps used here is based on that of Moraes et
al. (2022). More information about the synonyms and nomenclatural history of
the genus are available in Moraes et al. (2022: 316).

Julolaelaps gigas sp. nov.
https://Zoobank.org/FDD68D96-90DF-41 96-9DD5-377DCF03D633
Figs 1-16

Material examined. Holotype. REPUBLIC OF KOREA * 9; Sangju, Silkworm and
Insect Management Center; 36°57'N, 128°15'E; 19 May 2020; S. Keum leg.; on
captive giant African millipede, Archispirostreptus gigas (Spirostreptida: Spi-
rostreptidae); NIBRIV 0000905722. Paratypes. REPUBLIC OF KOREA * 29 26;
same data as for holotype; NIBRIV 0000905723, NIBRIV 0000905724, NIBRIV
0000905725, NIBRIV 0000905726.

Diagnosis. Dorsal shield smooth, without reticulation, bearing 22 pairs of
minute acicular setae, setae Z5 conspicuously longer than other setae on
shield, podonotal and opisthonotal parts of dorsal shield slightly hypotrichous,
setae in z- and s/S-series displaced laterally (on soft cuticle) and some missing
(z1, 26, J3); posterior margin of shield somewhat truncated; dorsal shield re-
duced, not covering entire idiosoma, opisthogastric and lateral soft cuticle with
37 pairs of setae, including 23 pairs of r-R-UR setae. Sternal shield reduced,
bearing only st7 and st2, eroded posteriorly, st3 and metasternal setae (st4) in-
serted on unsclerotized cuticle, epigynal shield drop-shaped, parapodal plates
broadly thickened, extending behind coxae IV, endopodal plates III/IV broadly
thickened, peritreme relatively long and rather broad, extending to anterior level
of coxa Il, cheliceral fixed digit with 2-3 teeth. Chaetotaxy of legs normal for
free-living Laelapidae, except tibia III with nine setae (two posterolateral setae

ZooKeys 1180: 51-65 (2023), DOI: 10.3897/zookeys.1180.109099 53

Omid Joharchi et al.: The genus Ju/olaelaps Berlese in Republic of Korea

Oo
idml Zl is
I i
AY

idmn4 @ads

Figures 1-5. Julolaelaps gigas sp. nov., female, with symbols for chaetotactic notation of idiosomal setae 1 dorsal idio-
soma 2 ventral idiosoma 3 subcapitulum 4 epistome 5 chelicera, lateral view.

ZooKeys 1180: 51-65 (2023), DOI: 10.3897/zookeys.1180.109099 54

Omid Joharchi et al.: The genus Ju/olaelaps Berlese in Republic of Korea

present) and genu IV with 10 setae (with two posterolateral setae). Male with
separate sternogenital and anal shields, chelicerae with edentate digits includ-
ing a regressed fixed digit and a stylet-like movable digit bordered by a very
long spermatodactyl.

Description. Female (N = 3). Figs 1-9, 12-14. Dorsal idiosoma (Figs 1, 12).
Length 906-925, width 620-649. Dorsal shield length 687-696, width 391-395,
posteriorly somewhat truncate, reduced, not covering entire idiosoma, some
dorsal setae left in the soft cuticle lateral to shield, becoming hypertrichous
cuticle surrounding dorsal shield, without distinct reticulate ornamentation over
whole surface; with 22 pairs of minute acicular setae, 13 pairs of podonotal se-
tae, plus nine pairs of setae on lateral soft cuticle ($7, s2, s6, r7-6), nine pairs of
opisthonotal setae, plus 21 pairs of setae on lateral soft cuticle (including S1-5
and R1-7); Zx, unpaired or asymmetrical setae and z7, z6, J3 absent, setae simi-
lar in length (9-15) and thicknesses; clonal setae Z5 (26-31) longer than other
setae on shield. Muscle insertions prominent as desclerotised circular patches.
Dorsal shield with 22 pairs of discernible pore-like structures, including only five
pairs of gland openings (gd7, gd4, gd6, gd8, gd9) and 17 pairs of poroids. Shape,
position and relative length and thicknesses of setae shown in Figs 1, 12.

Ventral idiosoma (Figs 2, 13). Tritosternum with paired pilose laciniae (105-
113), short base 30-35 x 23-27 wide; presternal platelets absent. Sternal shield
reduced (59-63 x 134-142 wide), shield with two pairs of smooth sternal se-
tae [st7, st2 (20-26)], and two pairs of poroids (iv7, iv2), eroded posteriorly,
surface without reticulate ornamentation, smooth, st3 (30-32) and metaster-
nal setae (st4, 29-31) inserted on soft integument, metasternal poroids (iv3)
apparently absent (Figs 2, 13), shield fused anterolaterally to narrow endopodal
strip between coxae | and II, endopodal plates III/IV broadly thickened (Figs 2,
13). Epigynal shield drop-shaped, with an obvious (narrow) neck at level of cox-
ae IV, protruding at level between setae st5 and Jv7, width (65-70) and length
(228-235), anterior and posterior margins rounded, with some irregular longi-
tudinal and oblique lines, otherwise relatively smooth, bearing a pair of simple
setae st5 (20-23) inserted on lateral margins of shield, near level of posterior
edge of coxae IV; paragenital poroids iv5 located on soft cuticle lateral to shield
near seta st5 (Figs 2, 13). Anal shield subtriangular, rounded anteriorly, length
133-138, width 108-114, surface without reticulate ornamentation, smooth,
para-anal setae (23-27) shorter than post-anal seta (30-35), cribrum well de-
veloped, with 3-4 irregular rows of spicules, each extending from cribrum to
near base of post-anal setae; anal opening located at anterior level of shield;
pair of glands gv3 inserted on shield lateral margins, at level para-anal setae
(Figs 2, 13). Soft opisthogastric cuticle surrounding epigynal and anal shields
with one pair of suboval metapodal plates (38-43 long x 13-18 wide) and sev-
en pairs of smooth setae (Jv7—Jv3, Jv5, Zv1—Zv3), setae more or less same in
length (18-24) and thickness (Figs 2, 13). Peritreme relatively long and broad,
extending to anterior level of coxa Il, peritrematal shield narrow, slightly expand-
ed anteriorly, each shield bearing three discernible pore-like structures, a gland
pore gp2 at level of coxa Ill, a lyrifissures jo3 and a gland pore gp3 on barely de-
veloped poststigmatic section (Figs 2, 13), anterior part of shield not fused with
dorsal shield; parapodal platelets broadly thickened, extending behind coxae IV,
bearing gland pore gv2; exopodal platelets absent (Figs 2, 13).

ZooKeys 1180: 51-65 (2023), DOI: 10.3897/zookeys.1180.109099 55

Omid Joharchi et al.: The genus Ju/olaelaps Berlese in Republic of Korea

all al2 all

Figures 6-9. Julolaelaps gigas sp. nov., female, with symbols for chaetotactic notation of legs setae 6 leg | (trochan-
ter-tibia, dorsal aspect) 7 leg II (trochanter-tibia, dorsal aspect) 8 leg III (trochanter-tarsus, dorsal aspect) 9 leg IV (tro-
chanter-tibia, dorsal aspect).

Gnathosomal structures (Figs 3-5, 14). Epistome triangular, with pointed
apex and smooth (Fig. 4). Hypostomal groove with six transverse rows of den-
ticles, each row with 3-5 denticles, with smooth anterior and posterior trans-

ZooKeys 1180: 51-65 (2023), DOI: 10.3897/zookeys.1180.109099 56

Omid Joharchi et al.: The genus Ju/olaelaps Berlese in Republic of Korea

verse lines (Fig. 3). Hypostome with four pairs of smooth setae, pc (24-26) >
h1 = h2 (18-21) > h3 (14-16) (Fig. 3). Corniculi robust and horn-like, extending
slightly beyond palpfemur. Internal malae with one pair of smooth median pro-
jections, flanked by lobes with fimbriate anterior margin; labrum with pilose
surface; supralabral process not distinct. Chaetotaxy of palps: trochanter 2,
femur 5, genu 6, tibia 14, tarsus 15, all setae smooth; palpfemur with seta d3
thickened and al paddle-like; palpgenu with a/7 stout, blunt, a/2 thickened and
spatulate; palptarsal apotele two-tined. Fixed digit of chelicera with 2-3 teeth
and long pilus dentilis, dorsal cheliceral seta relatively thick and short, arthrodi-
al membrane with a rounded flap and normal filaments; movable digit with two
mid-sized teeth (Figs 5, 14).

Insemination structures. Not seen, apparently unsclerotized.

Legs. (Figs 6-9). Legs II and III short (600-650, 625-655), | and IV longer
(657-680, 739-755). Chaetotaxy normal for free-living Laelapidae: Leg | (Fig.
6): coxa 0-0/1, 0/1-0, trochanter 1-0/1, 1/2-1, femur 2-3/1, 2/3-2, genu 2-3/2,
3/1-2, tibia 2-3/2, 3/1-2. Leg II (Fig. 7): coxa 0-0/1, 0/1-0, trochanter 1-0/1,
0/2-1, femur 2-3/1, 2/2-1, genu 2-3/1, 2/1-2, tibia 2-2/1, 2/1-2. Leg III (Fig. 8):
coxa 0-0/1, 0/1-0, trochanter 1-1/1, 0/1-1, femur 1-2/1, 1/0-1 (ad thickened
and inserted on small tubercles), genu 2-2/1, 2/1-1 (ad7 and pd7 inserted on
small tubercles), tibia: 2-1/1, 2/1-2. Leg IV (Fig. 9): coxa 0-0/1, 0/0-0, trochan-
ter 1-1/1, 0/1-1 (ad thickened), femur 1-2/1, 1/0-1 (ad7 longest, ad7 and ad2
inserted on small tubercles), genu 2-2/1, 3/0-2, tibia 2-1/1, 3/1-2. Tarsi II-IV
with 18 setae (3-3/2, 3/2-3 + mv, md); with some ventral and lateral setae thick-
ened. All pretarsi with well-developed paired claws, rounded pulvilli and nor-
mal ambulacral stalk.

Male (N = 2). Figs 10, 11, 15, 16. Dorsal idiosoma. Length 760-768, width
525-530. Dorsal shield length 647-653, width 345-350; ornamentation and
chaetotaxy as in female.

Ventral idiosoma. (Figs 10, 15). Sternal, genital, endopodal, ventral shields
fused into sternogenital shield, 327-333 long from anterior to posterior
margins of shield, 175-180 wide at level of st2, 160-165 at st3 level and
118-123 at st5 level; shield with six pairs of simple sternal setae (st7—5 and
Jv1) (19-30), and two pairs of poroids; anal shield free, length 117-123,
width 93-98, surface without reticulate ornamentation, smooth, post-anal
seta (25-28) slightly longer than para-anals (18-23), cribrum well devel-
oped, with 3-4 irregular rows of spicules, each extending from cribrum to
near base of post-anal setae; anal opening located at anterior level of shield;
pair of glands gv3 inserted on shield lateral margins, at level para-anal setae
(Figs 10, 15). Soft opisthogastric and lateral cuticle with 10-12 pairs of se-
tae. Peritremes, peritrematal shields and other ventral structures similar to
those in female.

Gnathosoma. (Figs 11, 16). Chelicerae with edentate digits including a re-
gressed fixed digit and a stylet-like movable digit bordered by a long sperm-
atodactyl, pilus dentilis long. Other gnathosomal structures similar to those
in female.

Legs. Chaetotaxy as in female.

Etymology. The name of this species refers to its occurrence on giant
African millipede of the species Archispirostreptus gigas (Spirostreptida:
Spirostreptidae).

ZooKeys 1180: 51-65 (2023), DOI: 10.3897/zookeys.1180.109099 BT

Omid Joharchi et al.: The genus Ju/olaelaps Berlese in Republic of Korea

Differential diagnosis. The female of the new species is unique within Julo-
laelaps because of its conspicuously reduced sternal shield, bearing only two
pairs of sternal setae (st7, st2), eroded posteriorly and endopodal plates III/IV

ZooKeys 1180: 51-65 (2023), DOI: 10.3897/zookeys.1180.109099 58

Omid Joharchi et al.: The genus Ju/olaelaps Berlese in Republic of Korea

Figures 12-16. Differential Interference Contrast (DIC) micrographs of Julolaelaps gigas sp. nov., female 12 idiosoma
in dorsal view 13 idiosoma in ventral view 14 chelicera in lateral view, male 15 idiosoma in ventral view 16 chelicera in
lateral view.

Zookeys 1180: 51-65 (2023), DOI: 10.: 59

Omid Joharchi et al.: The genus Ju/olaelaps Berlese in Republic of Korea

broadly thickened. In other features the new species is closest to J. vandaelen-
sis Maes, 1983 in having a genital shield narrower than anal shield, peritreme
almost reaching anterior margin of coxae II and dorsal shield with 22 pairs of
setae. It is distinguished from this species by the uniform minute acicular dor-
sal setae and the reduced dorsal shield, not covering entire idiosoma, leaving
an unsclerotised cuticle surrounding the dorsal shield.

Discussion

Casanueva (1993) redefined the family Laelapidae based on phylogenetic
evidence, merging the genera associated with millipedes (groups VI and VII,
see Casanueva 1993) with the genera associated with Araneae and Crustacea
(group VIII, fig. 7, p. 39), elevating the subfamily (Iphiopsidinae) to the level
of the family (Iphiopsididae). According to Casanueva (1993), the regressive
autopomorphy “absence of seta av2 on tibia |, see Casanueva 1993 attribute
#62” and “absence of seta p/2 on genu IV, see Casanueva 1993 attribute #58”
are the phylogenetic characters that define Iphiopsididae as a separate family
from Laelapidae. Based on attributes #58 and #62, the placement of the new
species (Julolaelaps gigas) in Iphiopsididae cannot be considered due to the
presence of both setae av2 and p/2 on tibia | and genu IV, respectively.

Moraza and Kazemi (2012) recognized three species groups within the ge-
nus, but the inclusion of Julolaelaps gigas sp. nov. requires some changes to
the diagnosis they introduced for each species group. Here we combine them
into two species groups and call them simply as follows: dispar and gigas spe-
cies groups. The dispar group includes species with largely complete dorsal
setae complement, with more than 29 setae pairs (at least series J and Z com-
plete), while the gigas species group is characterized by reduced dorsal setae,
with at most 25 setae pairs (at least series J and/or Z incomplete). Julolaelaps
buensis Maes, 1983 was not included in the key because the dorsal of the idio-
soma is not described due to poor fixation (Maes 1983). We have attempted to
provide diagnostic characters for each species and to classify each species as
either dispar or gigas. We stress that the information below was derived from
the descriptions only, and most of these species are in need of redescription.

Modified key to the species of Julolaelaps based on females (partly
from Moraza and Kazemi 2012), with emendations to add Julolaelaps
gigas sp. nov.

1 Dorsal shield setation hypotrichous, with at most 25 pairs of setae, at

least series J and/or Z incomplete (gigas species Group) ...........c:cceeeees 2
- Dorsal setation holotrichous or polytrichous, with more than 29 pairs of
setae, series J and Z usually complete (dispar species group) ............... 15

2 Sternal shield conspicuously reduced, bearing only two pairs of sternal
setae (st7, st2), endopodal plates III/IV broadly thickened ................c:c0e
Ferpeea tis tdehdirmnansh vere eco Astiahd Jas eal aera see ba den es Julolaelaps gigas sp. nov.

- Sternal shield well developed, bearing three pairs of sternal setae (st7-3),
if endopodal plates III/IV present not broadly thickened .................c cee 3

ZooKeys 1180: 51-65 (2023), DOI: 10.3897/zookeys.1180.109099 60

Omid Joharchi et al.: The genus Ju/olaelaps Berlese in Republic of Korea

3. Epigynal shield drop-shaped, with an obvious (narrow) neck at level of
coxae IV, narrower than anal shield; males with edentate chelicerae........ 4
- Epigynal shield well developed, wider than anal shield, males having den-

PATeSCMelICORaC. Se. ere lem eciue te rte tee bed nie A grata Uae eaten 13
4 Peritreme short, reaches at most to anterior level of coxa Ill .................... 5
- Peritreme long, reaches at least to level Of Coxa II... cece eeeereeees 10
5 Dorsal shield conspicuously reduced, with nine pairs of setae (including

ihree-opisthonotal pairs) scx, verte ieas ash ees we J. paucipilis Fain, 1987
- Dorsal shield with more than nine pairs Of Setae..............cccecesceesseeesseeeeees 6
6 Dorsal shield with 14 pairs of setae (including four opisthonotal pairs).......7
- Dorsal shield with 17-20 pairs Of S@tae@ ........ ec cececcsecescceseeecsseeessseeeenees 8

7 Marginal setae on dorsal shield conspicuously longer than central setae;
ventral setae simple; endopodal extension of sternal shield between coxae II
and III well developed; epistome smooth......... J. madiakokoensis Fain, 1987
- Marginal setae on dorsal shield as long as or slightly longer than central
setae; endopodal extension of sternal shield between coxae II and III ab-
SENT -CPISTOMESEILALC toc reute nM a eres y J. idjwiensis Fain, 1987
8 Dorsal shield with 17 pairs of setae (including six opisthonotal pairs).......
CER neg = ad ewirr Peeves ns AA TICS OPM PONS NSENT OMT ATES ot ARETE J. peritremalis Ryke, 1959
= Dorsal shieldiwith 19=20, palrs:0f SCTAC 5 ikeieecacceccedisvodecteseeteeendsh teaseenaeen 9
9 Dorsal shield with 19 pairs of smooth setae (including four opisthonotal
pairs), the central ones shorter than lateral ones, sternal shield deeply ex-
CAValeChOOSTCHIONY: © .ccx25 en, 28 WB, Pa, J. excavatus Fain, 1987
- Dorsal shield with 20 pairs of setae (including eight opisthonotal pairs)
heterogeneous in length, sternal shield straight posteriorly ..................0.
Pas Sie Fe Eas xn 27 FN See PT Re Or Co J. serratus Maes, 1983
10 Dorsal shield with 15 pairs of setae (including four opisthonotal pairs).....
eden Pedal ee Rook teh eee: J. celestiae Uppstrom & Klompen, 2005
- Dorsal shield with more than 15 pairs Of Setae........... eee eeeeeesteeenteeees 11
11 Dorsal shield with 20 pairs of minute setae (including eight opisthonotal
DAIS Ie re arassu etter pabcistessumvene cretuudy nosed eerste J. myriapodalis Ryke, 1959
- Dorsal shield with 22-25 pairs Of S@tae@ ........ eee cceseceesteeeseeeeteeeesseeees 12
12 Dorsal shield with 25 pairs of short setae, peritreme almost reaching to
mid-level of COXaeé I uo... eesee eee J. cameroonensis Maes, 1983
- Dorsal shield with 22, peritreme almost reaching anterior margin of coxae
Wancethe asses eycee tie Meare te se aan ae a ee ee J. vandaelensis Maes, 1983
13 Dorsal shield with 20 pairs of dorsal setae, setae j4 and 24 slightly longer

than other dorsomedial setae .................... J. parvitergalis Ishikawa, 1986
- Dorsal shield with more than 20 pairs of setae, setae j4, z4 conspicuously
longer than other dorsomedial Setae................cccccccccccsssseececesssseeeceessteeeeees 14

14 Dorsal shield with 22 pairs of setae, female cheliceral fixed digit with two
large teeth in addition to six-minute teeth .... J. nishikawai Ishikawa, 1986
- Dorsal shield with 23 pairs of setae, female cheliceral fixed digit with three
large teeth in addition to three small teeth... J. parvungulatus Ishikawa, 1986
15 Epigynal shield drop-shaped, with an obvious (narrow) neck at level of
coxae IV, narrower than anal shield...................... J. luctator Berlese, 1916
- Epigynal shield well developed, wider than anal shield .....................e 16

ZooKeys 1180: 51-65 (2023), DOI: 10.3897/zookeys.1180.109099 61

Omid Joharchi et al.: The genus Ju/olaelaps Berlese in Republic of Korea

16 Dorsal shield with 39-40 pairs of setae; setae j7 and Z5 conspicuously

longer than other dorsal setae; setae 27 and Z6 present...............::ceeeee 17
- Dorsal shield with 30-36 pairs of setae; setae z7 and/or z6 present or
LL) SSN Pera 9 Re rae Meee em, og sete ol ae rs Pete cote Sen ese ee nen See ee 19
17. Anal shield approximately twice as long as wide; para-anal setae at level
Of ANtEMOr MALGIN-Of ANUS e%r. 45%. fe cise. beeen J. dispar Berlese, 1916
- Anal shield nearly as long as wide; para-anal setae at level of posterior
IMAL O fe AIMS: tO A ee ee cee ese ns sae cee een tn nee on cake tee eet cee ae ea 18

18 Setae j/7 and Z5 subequal in length and longest dorsal setae; presternal
platelets absent; femur IV with one thickened dorsal seta, idiosoma 1180
LOG 2720 WIGS Secececewcececeseme Pecvcensi obinxaneeet: J. pararotundatus Ryke, 1959

- Setae j7 shorter than Z5; Z5 longest dorsal setae; presternal platelets
present; femur IV with two thickened dorsal setae; idiosoma 1000-1012

LONG ODO MWIGES, 5. sou ece cited aatelacccntes seen! J. spirostrepti Oudemans, 1914
19 Dorsal shield with 36 pairs of setae; setae z7, z6 and S7 always present;
setae Z5 twice as long aS f7 .......... eee J. moseri Hunter & Rosario, 1986
- Dorsal shield with 32-33 pairs of setae; setae 27, z6, r4, r6 absent and S7
DRESCMRON GO SeI ets ahs pelt chee sa raat ws con baiec usa ma erate ssaee iets oles 20
20 Dorsal shield with 32 pairs of setae; S7 absent; tritosternal base with ven-
tral disc-like structure................... J. tritosternalis Moraza & Kazemi, 2012

- Dorsal shield with 33 pairs of setae; S7 present; tritosternal base normal
and lacks ventral disc-like StrUCTUIe...............c:ccccccsssssceceessssccecesssesaeecsessaaeeees
Pence ever iacmien dete. Somers J. hallidayi Nemati, Riahi & Gwiazdowicz, 2015

Modified key couplet to the species of Julolaelaps based on known
males (after Moraza and Kazemi 2012)

14 Dorsal shield with 22 pairs of setae; peritreme reaching the middle of
COAG: WI 8 scan tentas SR eee RP AA Rca Sent a ate ade Arie igh ac arsk weenie, car een 15
- Dorsal shield with 25 pairs of short setae, peritremes extending to the
MIGdlE Of COXA Hh wr sn ccccecc ccibisyesccectuee czciuseys J. cameroonensis Maes, 1983
15 Sternal, genital, endopodal, ventral and anal shields fused into narrow ho-
lOVEM TRASH GA cccscnencraccamtrdetiies scsitins eSserbreatatin tes J. vandaelensis Maes, 1983
- Sternogenital and anal shields obviously Separated ............ eee eeeeseeeeteees
ree! hse SN IRE A aia te oR ok Ik iN oS OD ei inh 2B Julolaelaps gigas sp. nov.

Prior to this study, three species of Julolaelaps were reported on the African gi-
ant millipede, Archispirostreptus gigas (Peters) (Farfan and Klompen 2012): J. ce-
lestiae, J. kilifiensis and J. moseri. The native range of A. gigas is in Africa, and
the species has been moved throughout the world as part of the pet trade. So, if
mites in this genus are host-specific, Julolaelaps gigas must also be of African
origin, and has been moved around the world on its host. But most species of the
genus have been collected on only a few occasions, and the host species have
not been determined at the species level, making it difficult to draw firm conclu-
sions about their host specificity. The question of host specificity of the species
cannot be analyzed in detail until all available collections are re-examined to con-
firm their identification. On the contrary, Farfan and Klompen (2012) highlighted
a hypothesis suggesting that the presence of these mites on millipedes might
be linked to geographical location rather than host specificity. This implies that

ZooKeys 1180: 51-65 (2023), DOI: 10.3897/zookeys.1180.109099 62

Omid Joharchi et al.: The genus Ju/olaelaps Berlese in Republic of Korea

these mites could be specific to certain areas or types of off-host habitats. In
this scenario, a diverse range of hosts within the preferred habitat could serve as
suitable phoretic hosts. The intercontinental exchange and trade of millipedes,
accompanied by the transportation of mites and potential millipede contamina-
tion, complicates our ability to ascertain the true origin of this mite species.

The millipede from which the mites were collected was obtained from a pet
market where the import and breeding of exotic animals flourish as a business.
The second author observed that the millipede was mite-free when it got to the
Silkworm and Insect Management Center (Sangju, Republic of Korea) for an exhi-
bition. Nonetheless, all specimens of Julolaelaps gigas were discovered on cap-
tive giant African millipedes. The mystery remains regarding how these mites
came to inhabit this particular species. We need to do experiments to understand
the real ecological role of these mites, regardless of where they came from.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

The present study was fully supported by a grant from the National Institute of Biolog-
ical Resources (NIBR) funded by the Ministry of Environment (MOE) of the Republic
of Korea (NIBR202102203, NIBR202203202) and the National Research Foundation of
Korea (NRF-2018R1A6A1A03024862). Omid Joharchi’s study was also supported by
Cooperative Agreement No. FEWZ-2021-0004 from the Russian Ministry of Science
and Higher Education.

Author contributions

All authors have contributed equally.

Author ORCIDs

Omid Joharchi © http://orcid.org/0000-0002-2741-4946
Seoyoung Keum ® http://orcid.org/0000-0002-2219-9423
Chuleui Jung © http://orcid.org/0000-0001-8134-9279

Data availability

All of the data that support the findings of this study are available in the main text.

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