Molecular phylogeny of Acerentomidae (Protura), with

description of Acerentuloides bernardi sp. nov. from

North America
Julia Shrubovych1,2,*, Josef Starý3, and Cyrille A. D’Haese4

Abstract
The closely related genera Acerentulus Berlese, 1908 and Acerentuloides Ewing, 1921 are represented in the USA by only 3 species: Acerentulus confinis
(Berlese, 1908), Acerentulus christensoni (Ewing, 1940), and Acerentuloides americanus (Ewing, 1924). Study of proturan material from North America
yielded a new species belonging to Acerentuloides. The new species is characterized by the absence of seta sd4 on the head, presence of a minute api-
cal median seta on abdominal legs II and III, unique shape of maxillary gland with distal row of clustered globules, presence of setae modified as short,
thickened sensilla (sd5 on head, β1 and δ4 on foretarsus, setae P4 on metanotum and A2 on thoracic sterna, and accessory setae on tergites and ster-
nites I–VI), absence of seta P1a on abdominal tergites I–VI, foretarsal sensillum b longer than c, and presence of psl pores only on tergite VI. Molecular
sequences for several Acerentomidae, including A. confinis, were used to develop hypotheses about species relationships within Acerentomidae.

Key Words: Acerentulus; Podolinella; Indiana; USA; DNA barcoding; phylogeny

Resumen
Los géneros Acerentulus Berlese, 1908 y Acerentuloides Ewing, 1921, muy relacionados entre sí, están representados en Estados Unidos por sólo 3
especies: Acerentulus confinis (Berlese, 1908), Acerentulus christensoni (Ewing, 1940) y Acerentuloides americanus (Ewing, 1924). El estudio del ma-
terial de proturas de Norteamérica resulto en una nueva especie perteneciente a Acerentuloides. La nueva especie se caracteriza por la ausencia de
seta sd4 en la cabeza, la presencia de una seta muy corta en el apice central de las patas abdominales II y III, la forma única de la glándula maxilar con
una hilera distal de glóbulos agrupados, la presencia de setas modificadas como sensilas cortas y gruesas (sd5 en cabeza, β1 y δ4 en tarso anterior,
setae P4 en el metanotu y A2 en esternón torácico y setas accesorias en tergitos y esternitos I-VI), ausencia de seta P1a en tergitos abdominales I-VI,
sensillum b de primer tarso más largo que c, y la presencia de poros psl solamente en el tergito VI. Se utilizaron secuencias moleculares para varios
Acerentomidae, incluyendo A. confinis, para desarrollar la hipótesis sobre las relaciones de especies dentro de Acerentomidae.

Palabras Clave: Acerentulus; Podolinella; Indiana; Estados unidos; códigos de barras de ADN; filogenia

The history of the work on the genus Acerentuloides (Entognatha: phologically similar genus Acerentulus comprises 49 species (Szeptycki
Protura: Acerentomidae), especially of its type species, Acerentuloides 2007; Wu & Yin 2007; Shrubovych et al. 2012, 2014b; Galli & Capurro
americanus (Ewing, 1924), is worth examining. The genus was originally 2013) and is distributed worldwide, but in North America only 2 spe-
described by Ewing (1921) with Acerentuloides bicolor Ewing, 1921 as cies are known: Acerentulus confinis (Berlese, 1908) and Acerentulus
its type species. The species A. americanus was originally described by christensoni (Ewing, 1940). In the present paper, we describe a sec-
Ewing (1924) as Acerentomon americanum (Ewing, 1924). Acerentomon ond species of Acerentuloides, provide a generic diagnosis, and discuss
americanum was transferred to the genus Acerentulus after revision of the phylogenetic position of the genus Acerentuloides, subfamily Ber-
Ewing’s type material of Protura (Hilton 1943; Bonet & Tuxen 1960). berentulinae and family Acerentomidae within Acerentomata.
Tuxen (1963) created for this species the new genus Amerentulus Tuxen,
1963 with the type species Amerentulus americanus (Ewing, 1924), de-
spite the fact that type material was lost and Tuxen had doubts about Materials and Methods
the validity of the new genus (Tuxen 1964, p. 225). Nosek & McEwan
Kevan (1984, p. 59), studying Canadian specimens of A. americanus, re- Material of the new species was collected in the framework of a soil
established the generic name of Acerentuloides and synonymized it with biota study in post-mining sites in the USA (Frouz et al. 2013). Samples
Amerentulus, with the type species Acerentuloides americanus. were collected from litter and rhizosphere of deciduous forest with
The genus Acerentuloides contains only the single species A. ameri- dominant black locust tree (Robinia pseudoacacia L.; Fabaceae) and
canus, distributed in the USA and Canada (Szeptycki 2007). The mor- red oak (Quercus rubra L.; Fagaceae). The forest patch is a 16-yr-old

1
Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Sławkowska 17, Cracow, Pl 31-016, Poland; E-mail: shrubovych@gmail.com (J. Sh.)
2
State Museum of Natural History, Ukrainian National Academy of Sciences, Teatral’na 18, Lviv, UA 79-008, Ukraine
3
Biology Centre v.v.i., Academy of Sciences of the Czech Republic, Institute of Soil Biology, Na Sádkách 7, CZ-37005 České Budějovice, Czech Republic;
E-mail: jstary@upb.cas.vz (J. St.)
4
MECADEV, UMR7179 CNRS MNHN, Muséum National d’Histoire Naturelle, CP50 Entomology, 45 rue Buffon, 7505 Paris, France; E-mail: dhaese@mnhn.fr (C. A. D.)
*Corresponding author: E-mail: shrubovych@gmail.com (J. Sh.)

2017 — Florida Entomologist — Volume 100, No. 2 433

434 2017 — Florida Entomologist — Volume 100, No. 2
re-growth after coal mining in the Patoka River National Wildlife Ref- Phylogenetic affinities were analyzed by comparing the obtained
uge and Management Area near the Hugh Boyd Fishing Pier & Wildlife COI, 18S rRNA, 28S rDNA D1–D2, and 28S rDNA D3–D6 sequences
Observation Deck, near Oakland City, Gibson County, Indiana. Speci- with sequences of other members of Acerentomidae published in
mens of A. confinis were collected from leaf litter at the base of white previous works (Shrubovych et al. 2012, 2014b,c, 2016; Resch et al.
oak in woods in Calhoun, McMinn County, Tennessee (35.295833°N, 2014) completed with published sequences (Bu & Wu 2012; Bai &
84.748056°W), on 6 Aug 2013 by E. C. Bernard and K. J. Whitlock. The Bu 2013) and other unpublished sequences found in BOLD (Table
specimens were extracted from soil and moss samples with a Ber- 1). Other Acerentomata genera (Neocondeellum [Protentomidae],
lese–Tullgren funnel into 95% ethanol. Specimens were mounted on Proturentomon [Protentomidae], and Hesperentomon [Hesperen-
microscope slides in Marc André II medium (Massoud 1967) and were tomidae]) were used to root the trees (see Table 1). Some of the COI
examined with a compound microscope with differential interference sequences downloaded from GenBank or the Barcode of Life Data
contrast optics at magnifications ranging from 250× to 1000×. Draw- System (BOLD) were shorter than the barcode 658 bp so the miss-
ings were made with a drawing tube. Specimens for scanning electron ing ends of the alignment were completed with Ns. Sequences were
microscopy (SEM) observations were preserved in 100% ethanol be- aligned, for each locus independently, using MUSCLE v3.8.31 with
fore critical point drying (Emitech K850, Quorum Technologies Ltd, default parameters (Edgar 2004).
Laughton, England) and sputter gold coating, and imaged with a Jeol Maximum likelihood (ML) analyses were performed using the par-
JFC-1200 (JEOL Ltd, Tokyo, Japan) scanning electron microscope. titioned ML method in RaxML (Stamatakis 2014) through the graphical
All synonymies, systematics, and literature data up to 2006 are interface raxmlGUI v1.5 (Silvestro & Michalak 2012). A thorough ML
given in Szeptycki (2007). Head seta designations follow Rusek et al. tree search was conducted with the GTR + Г+ I model through 10 runs,
(2012); terminology for body chaetotaxy and porotaxy follows Szep- and nodal branch support was evaluated with 1,000 bootstrap repli-
tycki (1988, 1993) and Shrubovych (2014), body indices (PR, CF, BS, cates (+BS brl). Identical sequences were not omitted for the analysis.
TR, EU) follow Tuxen (1964). Abbreviations used in the description are Parsimony under dynamic homology was performed using POY v5.1.2
as follows: Abd = abdominal segments, al = anterolateral pore, cp = (Wheeler et al. 2015) for 9 gap:transversion:transition Sankoff matrices
clypeal pore, fp = frontal pore, psl = posterosublateral pore, psm = pos- ranging from 1:1:1 to 16:4:1 (for a detailed procedure, see Schneider &
terosubmedial pore, spm = sternal posteromedial pore, spsm = sternal D’Haese 2013). All trees were visualized using Figtree v1.4.2 (Rambaut
posterosubmedial pore, Th = thoracic segments. & Drummond 2010).
In addition to the morphological description, the DNA barcode
sequences were amplified to enhance the description (Stevens et al.
2011). DNA was extracted from 95% ethanol preserved specimens with Results
a Qiagen DNeasy tissue extraction kit (Qiagen, Hilden, Germany). The
specimens were digested overnight in buffer + proteinase k solution, The genus Acerentuloides is characterized by 2 pairs of A-setae on
and the extraction was carried out according to the manufacturer’s the mesonotum and metanotum; 3 setae on the 2nd and 3rd pair of
recommendations with final re-suspension in 125 µL of the elution buf- abdominal legs, of which the apical median seta is minute; well devel-
fer. The voucher specimens were then retrieved, further cleared in lac- oped labial palpus with terminal tuft of setae and broadened sensil-
tic acid solution for approximately 24 h, and mounted on microscope lum; maxillary gland with small, smooth, globular vesicle or granulated
slides in Marc André II mounting medium. Polymerase chain reaction appendix on the calyx and with several small globules in distal part;
(PCR) for DNA amplification was carried out in a 25µL volume reaction some setae modified as short, thickened sensilla (sd5 on head; β1 and
with Taq-&LOADTM Mastermix 5xC reagent (MP Biomedicals, Santa Ana, δ4 on foretarsus; setae P4 on metanotum, M2 on prosternum, and
California). The thermocycler program consisted of an initial denatur- A2 on thoracic sterna; and accessory setae on tergites and sternites I–
ing step at 94 °C for 2 min, 5 amplification cycles with a 45 °C annealing VI); 6 setae on sternite VIII; anterior position of seta P3 on abdominal
temperature (94 °C for 40 s, 45 °C for 40 s, 72 °C for 1 min), 30 cycles tergites II–VI; developed striate band with clearly visible parallel-sided
with a 51 °C annealing temperature, and a final extension step at 72 striae. Foretarsal sensillum t1 is claviform, sensillum t3 is long and
°C for 5 min. lancet-like (Bonet & Tuxen 1960) or finger-like, sensillum b’ is present,
The PCR amplification and sequencing were carried out with primers the base of sensillum d is closer to base of c than to base of e, and the
newly designed for Protura: LCOprot (5’-TTT CTA CTA ATC ATA AGG ATA position of sensillum a’ is close to the base of t1.
TTG G-3’) and HCOprot (5’-TAN ACY TCW GGR TGS CCA AAR AAT CA-3’).
We also selected 3 other loci to amplify for the phylogenetic analyses:
Acerentuloides bernardi Shrubovych sp. nov., 2016 (Figs. 1–34;
18S rRNA and 28S rDNA (regions D1–D2 and D3–D6) nuclear ribosomal
DNA. The 18S rRNA loci were PCR amplified in 3 overlapping fragments Table 2)
using primer pairs 1F + 5R, 3F + 18Sbi, and 5F + 9R (e.g., Giribet et al.
2004). For the 28S rDNA regions, details are described in Schneider & TYPE MATERIAL
D’Haese (2013) and Stevens & D’Haese (2014), and several primer pairs The type materials were deposited in the collection of the Institute
were used combining Collembola and Protura specific primers (some of Systematics and Evolution of Animals of the Polish Academy of Sci-
newly designed for the present work): 28S-C1c (5’-ACC CGC YWA ATT ences (ISEA), Cracow, Poland, and in the collection of the State Mu-
TAA GCA T-3’) and 28S-ApR (5’-CGT GTT TCA AGA CGG GYC-3’) for 28S seum of Natural History (SMNH) of the National Academy of Sciences
rDNA D1–D2; and 28S-Ap (5’-GRC CCG TCT TGA AAC ACG-3’) and 28S- of Ukraine, L’viv, Ukraine.
D4D5R (5’-GTT ACA CAC TCC TTA GCG GA-3’) for 28S rDNA D3–D6. HOLOTYPE 1 female (ISEA 6647) USA: Indiana, Oakland City, Hugh
The PCR products were sequenced by Eurofins (Paris, France). Re- Boyd, Patoka River National Wildlife Refuge and Management Area,
sulting chromatograms were interpreted using the program Sequench- 9-V-2008, latitude 38.3539°N, longitude 87.3156°E, elevation 133 m,
er 4.5 (Gene Codes Corporation, Ann Arbor, Michigan) or CodonCode deciduous growth with dominant black locust tree (Robinia pseudo-
Aligner 6.0.2 (CodonCode Corporation, Centerville, Massachusetts). acacia L.; Fabaceae) and red oak, sample of litter and rhizosphere, col-
Sequences were manually checked for misreadings of the chromato- lected by J. Tajovský & J. Frouz.
grams. PARATYPES 2 females (ISEA 6648, SMNH 89.1), data same as holotype.
Table 1. List of investigated proturans and accession numbers of gene sequences used in the phylogenetic analysis (a dash indicates that the gene sequence was not available).

Species namea 28S rDNA D3–D6 28S rDNA D1–D2 COI 18S rRNA Family Subfamily
Proturentomon chinense EU557257 EU557257 HQ882814 EU557244 Protentomidae Protentominae
Neocondeellum brachytarsum EU557259 EU557259 HQ882816 EU557245 Protentomidae Condeellinae
Neocondeellum dolichotarsum EU557258 EU557258 HQ882815 — Protentomidae Condeellinae
Hesperentomon nanshanensis — — KF530828 — Hesperentomidae Hesperentominae
Hesperentomon pectigastrulum EU557255 EU557255 HQ882812 EU557242 Hesperentomidae Hesperentominae
Hesperentomon yangi — — KF530824 — Hesperentomidae Hesperentominae
Acerella muscorum HQ882811 HQ882811 HQ882825 HQ882809 Acerentomidae Acerellinae
Acerella muscorum KJ101608 — — KJ101608 — Acerentomidae Acerellinae
Acerentomon carpaticum PROTA003 PROTA003-15 PROTA003-15 PROTA003-15 — Acerentomidae Acerentominae
Acerentomon carpaticum PROTA006 PROTA006-15 PROTA006-15 PROTA006-15 — Acerentomidae Acerentominae
Acerentomon carpaticum PROTA007 PROTA007-15 PROTA007-15 PROTA007-15 — Acerentomidae Acerentominae
Acerentomon dispar PROTA001 PROTA001-15 PROTA001-15 PROTA001-15 — Acerentomidae Acerentominae
Acerentomon dispar PROTA009 PROTA009-15 PROTA009-15 PROTA009-15 — Acerentomidae Acerentominae
Acerentomon dispar PROTA023 PROTA023-15 PROTA023-15 PROTA023-15 — Acerentomidae Acerentominae
Acerentomon dispar PROTA024 PROTA024-15 PROTA024-15 PROTA024-15 — Acerentomidae Acerentominae
Acerentomon dispar PROTA025 PROTA025-15 PROTA025-15 PROTA025-15 — Acerentomidae Acerentominae
Acerentomon italicum PROAT052 PROAT052-12 PROAT052-12 PROAT052-12 — Acerentomidae Acerentominae
Acerentomon maius PROAT001 PROAT001-12 PROAT001-12 PROAT001-12 — Acerentomidae Acerentominae
Acerentomon maius PROAT005 PROAT005-12 PROAT005-12 PROAT005-12 — Acerentomidae Acerentominae
Acerentomon maius PROAT017 PROAT017-12 PROAT017-12 PROAT017-12 — Acerentomidae Acerentominae
Acerentomon maius PROAT024 PROAT024-12 PROAT024-12 PROAT024-12 — Acerentomidae Acerentominae
Acerentomon microrhinus HQ8828 HQ882810 HQ882810 HQ882819 HQ882808 Acerentomidae Acerentominae
Acerentomon microrhinus JQ728012 — — JQ728012 — Acerentomidae Acerentominae
Acerentomon christiani PROAT026 PROAT026-12 PROAT026-12 PROAT026-12 — Acerentomidae Acerentominae
Acerentomon christiani PROAT027 PROAT027-12 PROAT027-12 PROAT027-12 — Acerentomidae Acerentominae
Acerentomon christiani PROAT034 PROAT034-12 PROAT034-12 PROAT034-12 — Acerentomidae Acerentominae
Acerentomon christiani PROAT035 PROAT035-12 PROAT035-12 PROAT035-12 — Acerentomidae Acerentominae
Acerentomon christiani PROAT036 PROAT036-12 PROAT036-12 PROAT036-12 — Acerentomidae Acerentominae
Acerentomon christiani PROAT040 PROAT040-12 PROAT040-12 PROAT040-12 — Acerentomidae Acerentominae
Acerentomon christiani PROAT055 PROAT055-12 PROAT055-12 PROAT055-12 — Acerentomidae Acerentominae
Acerentomon christiani PROAT064 PROAT064-12 PROAT064-12 PROAT064-12 — Acerentomidae Acerentominae
Acerentomon christiani PROAT071 PROAT071-12 PROAT071-12 PROAT071-12 — Acerentomidae Acerentominae
Acerentomon spgr microrhinus PROAT022 PROAT022-12 PROAT022-12 PROAT022-12 — Acerentomidae Acerentominae
Acerentomon sp JX963616 — — JX963616 — Acerentomidae Acerentominae
Filientomon takanawanum EU557261 EU557261 HQ882822 EU557249 Acerentomidae Acerentominae
Huashanentulus huashanensis EU557262 EU557262 HQ882821 EU557248 Acerentomidae Acerentominae
Yamatentomon guoi YYH45 — — JQ846460 — Acerentomidae Acerentominae
Yamatentomon guoi YYH46 — — JQ846461 — Acerentomidae Acerentominae
Yamatentomon guoi YYH47 — — JQ846462 — Acerentomidae Acerentominae
Acerentulus charrieri cs59 ABPE002-17 ABPE002-17 — JQ411216 ABPE002-17 Acerentomidae Berberentulinae
Acerentulus charrieri cs64 ABPE003-17 ABPE003-17 — JQ411217 — Acerentomidae Berberentulinae
Acerentulus confinis p029 ABPE004-17 — ABPE004-17 ABPE004-17 ABPE004-17 Acerentomidae Berberentulinae
Acerentulus noeli csp06 ABPE005-17 ABPE005-17 ABPE005-17 KJ210840 ABPE005-17 Acerentomidae Berberentulinae
Acerentulus noeli csp13 ABPE006 — — KJ210841 — Acerentomidae Berberentulinae
a
Extension after the species name corresponds to the specimen voucher code.
Shrubovych et al.: Molecular phylogeny of Acerentomidae, Acerentuloides bernardi sp. nov. 435
 436 2017 — Florida Entomologist — Volume 100, No. 2
DESCRIPTION

Nipponentominae
Habitus typical for members of Acerentomidae (Fig. 24). Head

Berberentulinae
Berberentulinae
Berberentulinae
Berberentulinae
Berberentulinae
Berberentulinae
Berberentulinae
Berberentulinae

Berberentulinae
Berberentulinae
setae short, cephalic seta l3 setiform (Figs. 1 and 2), seta sd5 thick,
Subfamily

sensilliform (Figs. 1 and 3), setae sd4 and d6 absent, length ratio of
posterior setae d7:sd7 as 1.0:1.5 (Fig. 1). Pseudoculus circular, with
short posterior extension, PR = 14 (Fig. 2). Maxillary palpus apically
with tuft of setae and 4 single setae, basal sensilla slender, subequal
Table 1. (Continued) List of investigated proturans and accession numbers of gene sequences used in the phylogenetic analysis (a dash indicates that the gene sequence was not available).

in length (Fig. 4). Labial palpus well developed with 4-branched api-
cal tuft and sausage-shaped basal sensillum (Figs. 5 and 25). Maxil-
lary gland with small elongated and weakly granulated calyx and

Acerentomidae
Acerentomidae
Acerentomidae
Acerentomidae
Acerentomidae
Acerentomidae
Acerentomidae
Acerentomidae
Acerentomidae

Acerentomidae
Acerentomidae

small globular vesicles on calyx, long posterior filament with row

Family

of small globules posteriorly ending in bilobed dilation, CF = 3.7

(Fig. 6).
Foretarsus with sensillum b’ present, t1 claviform, t3 long and fin-
ger-like, all other sensilla slender and parallel-sided (Figs. 9, 10, and
26). Sensillum a reaching base of t2. Sensillum b longer than c, extend-
— aExtension after the
species name corresponds
to the specimen voucher

ing past base of sensillum e. Sensillum c reaching base of sensillum

e. Sensillum b inserted proximally to c, sensillum d inserted between
ABPE010-17
ABPE008-17
18S rRNA

EU557251
EU557246
EU557247

sensilla c and t2. Sensillum a’ short, extending past base of t2 (Fig.

AY037169
—
—
—
—

26). Sensillum b’ reaching base of sensillum c’, apex of sensillum c’ not

reaching base of claw. Length formula of sensilla: t1 < t3 < (a’ = b’) < (g =
c’) < (c = t2) < e < (a = d) < b < f. Setae β1 and δ4 modified, sensilliform,
code.

shorter than other δ-setae (length of β1 = 4 μm, δ4 = 6 μm). Pores on

foretarsus near base of sensillum t3 and between bases of sensillum
c and seta α3. Claw short, without inner tooth, empodial appendage
short. BS = 0.6, TR = 3.6, EU = 0.12.
HQ882823
HQ882818
HQ882817
HQ882820

KJ395313
KJ395311
KJ395312
KJ210839
KJ210842

KJ210838

Formula of chaetotaxy given in Table 2. Setae on nota strongly

COI

differing in length. Pronotal seta 1 twice the length of seta 2 (Fig.

11). Meso- and metanotal setae P1a and P2a very short, oblong
(Fig. 27), P2a situated close to P3, seta P5 gemmate (Figs. 11 and
12). Length ratio of mesonotal setae P1:P2 = 1.0:1.6. Seta P4 on
metanotum a short sensillum, length 3 μm (Fig. 12). Meso- and
metanota with sl and al pores (Figs. 11 and 12). Thoracic sterna
28S rDNA D1–D2

ABPE010-17

without pores. Setae A2 and M2 on prosternum and seta A2 on

EU557263
EU376049
EU557260

EF192435
EF192433
ABPE009

thoracic sterna short, sensilliform; length of prosternal A2 = 3 μm,

—
—
—

of prosternal M2 = 1 μm (Figs. 28 and 29), of meso- and metasternal

A2 = 1 μm (Figs. 13–15).
Setae A5 and P2a on tergite I, setae P2a and P4a on tergites
II–VI short and sensilliform, their length 3 μm (Figs. 16, 17, and 30).
Accessory setae P1a, P2a, and P4a on tergite VII setiform, longer,
28S rDNA D3–D6

length 4 μm (Fig. 18). Seta P3 on tergites II–VI inserted anteriorly to

ABPE010-17
ABPE007-17

ABPE008-17

Extension after the species name corresponds to the specimen voucher code.

other setae of P-row (Fig. 17), P3 on tergites I and VII level with oth-
EU557263
EU376049
EU557260

EF192435
EF192433

er setae of P-row (Figs. 16 and 18). Tergites VI–VII with connecting

—
—
—

line in anterior part (Figs. 17 and 18). Pores psm present on tergites
I–VII between setae P1 and P2, and close to seta P1a on tergite VII,
al pores on tergites II–VII, psl pores on tergite VI only (Figs. 16–18).
Abdominal legs with 4, 3, 3 setae. Subapical seta on 2nd and 3rd
pairs of abdominal legs nearly twice the length of apical lateral seta
(21 and 12 μm, respectively). Apical median seta minute, length 1
μm (Figs. 21 and 31). Accessory setae P1a on sternites I–VI sensil-
Andinentulus rapoporti csp20 ABPE011-17
Andinentulus rapoporti csp16 ABPE009-17
Andinentulus rapoporti csp19 ABPE010-17
Acerentulus pyreneicus csp10 ABPE008-17

liform, on sternite VII setiform, short, P1a length on sternites I‒VII 3

μm (Figs. 20, 22, 23, and 31–33). Sternites VI–VII with a connecting
Acerentulus noeli csp14 ABPE007-17

line in anterior region (Figs. 22 and 23). Sternites II–V with asym-
metrical spsm pore (Fig. 20). Sternite VI with spsm pores, 2 near
Baculentulus tienmushanensis
Acerentulus pyreneicus csp11

each other and 1 close to base of seta P1 (Figs. 22 and 32); sternite
Gracilentulus maijiawensis

VII with spm pore (Fig. 23) or in 1 paratype with asymmetrical spsm
Baculentulus densus
Acerentulus sinensis

pore between setae P1 and P1a (Fig. 33).

Nosekiella sinensis

Abdominal segment VIII with well-developed striate band (Figs.

Species namea

19 and 34). Pore psm without accompanying teeth (Fig. 19). Posterior
margin of sternite VIII and laterotergites smooth (Figs. 23 and 34).
Comb on tergite VIII with 8–9 short teeth (Fig. 7). Sternites IX–XII with
a

smooth hind margin; setae 1 about one-third length of setae 2 (Figs.

Shrubovych et al.: Molecular phylogeny of Acerentomidae, Acerentuloides bernardi sp. nov. 437

Figs. 1–10. Acerentuloides bernardi sp. nov. 1. Head, right side; 2. pseudoculus with seta l3; 3. cephalic seta sd5; 4. maxillary palpus; 5. labial palpus; 6. maxillary
gland; 7. comb; 8. female squama genitalis; 9. foretarsus, exterior view; 10. foretarsus, interior view. Arrows indicate pores (cp = clypeal pore, fr = frontal pore).
Scale bars: 20 µm.

23 and 34). Segment XII with medial pore on dorsal lobe and pair of ETYMOLOGY
sternal anterolateral pores.
The new species is cordially dedicated to our colleague and emi-
Female squama genitalis with short, forked acrostyli (Fig. 8). Males
nent zoologist, Prof. Dr. Ernest C. Bernard.
unknown.
Body measurement (3 females): body length 1,100 μm; head 130–
134 μm; pseudoculus 9 μm, lever 1 μm; posterior part of maxillary
REMARKS
gland 35 μm; head setae d7 = 11 μm, sd7 = 16 μm, l3 = 6 μm; pronotal The habitus of the new species is very similar to A. confinis (Figs.
setae 1 = 25 μm, 2 = 12 μm, mesonotal setae P1 = 19–20 μm, P1a = 1 24 and 35). The species is characterized by absence of seta sd4 and
μm, P2 = 30–31 μm; foretarsus 90 μm, claw 25 μm, empodial append- additional seta d6 on head, absence of seta P1a on abdominal tergites
age 3 μm. I–VI, presence of seta Pc on sternite VII, short sensillum a reaching to
438 2017 — Florida Entomologist — Volume 100, No. 2

Figs. 11–15. Acerentuloides bernardi sp. nov. 11. Pronotum and mesonotum, right side; 12. lateral part of metanotum; 13. anterior part of prosternum; 14. an-
terolateral part of mesosternum; 15. anterolateral part of metasternum. Arrows indicate pores (al = tergal anterolateral, sl = tergal sublateral). Scale bars: 20 µm.

the base of sensillum t2, long foretarsal sensilla b and f, sensillum c quences were deposited in BOLD under accession numbers ABPE002-
shorter than b, short and slender sensilla a’, b’ and c’, and presence of 17-ABPE011-17 (see Table 1).
psl pores on tergite VI only. Acerentuloides bernardi sp. nov. is similar The concatenated data (COI, 18S rRNA, 28S rDNA D1–D2, and 28S
to A. americanus in the shape of the maxillary gland, presence of a rDNA D3–D6) consist of a total alignment length of 4,438 bp for 55 ter-
minute apical medial seta on abdominal legs II and III, shape of the minal taxa (27 species). The ML inference and direct optimization parsi-
comb and the length of foretarsal setae a, b’ and c’ (Ewing 1921, 1940; mony phylogenies all showed consistent agreement among topologies.
Bonet & Tuxen 1960). The new species differs in possessing seta Pc on The only real difference is the position of Nosekiella+Huashanentulus
sternite VII and in the shape of foretarsal sensillum t3 (lancet-like in sister group of Acerella in the ML analysis and sister group of the rest
A. americanus, finger-like in the new species). Foretarsal sensillum b of Acerentominae in parsimony. Here we show the ML tree (Fig. 41).
is longer than c and clearly surpasses the base of seta γ3 in the new
species, whereas in A. americanus sensillum b is shorter and does not
reach the base of γ3; in Canadian specimens of A. americanus sensilla Discussion
b and c are of equal length (Nosek & McEwan Kevan 1984) and sensil-
lum a’ is longer and extends past the base of sensillum t2. In addition, Tuxen created the genus Amerentulus Tuxen, 1963 (currently
the new species has a smooth, globular vesicle on the maxillary gland, Acerentuloides [Ewing, 1921]) on the basis of 2 differentiating pe-
whereas Canadian specimens of A. americanus have a granulated ap- culiarities: the minute apical medial setae on 2nd and 3rd pairs of
pendix on the calyx (Nosek & McEwan Kevan 1984). abdominal legs and the presence of a distal row of globules on the
maxillary gland. The species described in the present paper is char-
acterized by the absence of cephalic setae sd4, which is present in
MOLECULAR ANALYSIS all Acerentulus species (see Fig. 36, American specimen of type spe-
Unfortunately, DNA was not retrieved from specimens of A. ber- cies A. confinis [Berlese, 1908]). So far, this characteristic has been
nardi sp. nov. However, the sequencing of A. confinis, a species from observed only in the monotypic genera Podolinella Szeptycki, 1995
a closely related genus, was successful. A 658 bp fragment of the COI and Maderentulus Tuxen, 1963 (Tuxen 1982, fig. 1). Szeptycki (1995)
gene (DNA barcode) as well as 1,541 bp of the 18S rRNA and 971 bp stated this characteristic in his generic diagnoses. Therefore, the ab-
of the 28S rDNA D1–D2 were amplified and sequenced from a speci- sence of this seta could be an additional morphological character for
men collected in the USA. To complete the COI data sets previously Acerentuloides or perhaps only for A. bernardi sp. nov. The genus
published (Shrubovych et al. 2012, 2014b, 2014c), other Acerentulus Podolinella differs from Acerentuloides in that abdominal legs II and
and Andinentulus species were amplified for 18S rRNA: Acerentulus III have only 2 setae and the labial palpus is reduced to a sensillum
charrieri Shrubovych, Schneider & D’Haese, 2012, A. noeli Shrubovych, and 3 setae. Maderentulus differs from Acerentuloides in the shape
Schneider & D’Haese, 2014., A. pyreneicus Shrubovych, Schneider & of abdominal legs II and III with 2 setae and shape of foretarsal sen-
D’Haese, 2014, and Andinentulus rapoporti (Condé, 1963); 28S rDNA silla t1 (filiform) and t3 (cylindrical). The new species is character-
D1–D2: A. noeli and Andinentulus rapoporti (2 different specimens); ized by having a finger-like foretarsal sensillum t3, which differs from
28S rDNA D3–D6: A. charrieri (2 different specimens), A. noeli (2 dif- the leaf-like shape of this sensillum in Acerentulus species, such as in
ferent specimens), A. pyreneicus, and Andinentulus rapoporti. The se- American specimens of A. confinis (Fig. 37).
Shrubovych et al.: Molecular phylogeny of Acerentomidae, Acerentuloides bernardi sp. nov. 439

Figs. 16–23. Acerentuloides bernardi sp. nov. 16. Tergite I, right side; 17. tergite VI, right part; 18. tergite VII, right part; 19. tergite VIII; 20. sternite II; 21. abdominal
leg of sternite II; 22. sternite VI; 23. sternites VII–IX. Arrows indicate pores (psm = tergal posterosubmedial, psl = tergal posterosublateral, spsm = sternal postero-
submedial, spm = sternal posteromedial). Scale bars: 20 µm.
440 2017 — Florida Entomologist — Volume 100, No. 2

Figs. 24–34. Acerentuloides bernardi sp. nov. scanning electron microscopy photographs. 24. Habitus; 25. labial palp (apical tuft with 4 setae broken; s = labial
sensillum); 26. foretarsus, interior view: sensilla t1, t3 and a’; 27. modified seta P2a on mesonotum; 28. modified seta A2 on prosternum; 29. modified seta M2 on
prosternum; 30. modified seta A5 on tergite I and P1a on sternite I; 31. abdominal leg on segment III (sa = subapical, am = apical medial, al = apical lateral setae;
apical lateral seta is broken); 32. hind margin of sternite VI; 33. hind margin of sternite VII; 34. sternites VIII–XII. Scale bars = 300 µm (Fig. 24), 4 µm (Figs. 25 and
27–29), 10 µm (Fig. 31), and 20 µm (Figs. 26, 30, and 32–34).

Porotaxy of the new species is typical for species of Acerentulus. such as Acerentulus Berlese, 1908, Andinentulus Tuxen, 1984, Austral-
The presence of psl pores on tergite VI and absence on tergite VIII may entulus Tuxen, 1967, Brasilidia Nosek, 1973, Najtentulus Szeptycki &
be specific features of A. bernardi sp. nov., but the porotaxy of Aceren- Weiner, 1997, and Fjellbergella Nosek, 1978. Within this group Aceren-
tulus species is not well known. The porotaxy of A. americanus was not tulus and Najtentulus are characterized by a well developed labial pal-
described, but Bonet & Tuxen (1960, pp. 283, 285) identified accessory pus with an apical tuft of setae (Fig. 38), 6 setae and well-developed
setae P1a on tergites anterior to the posterior setae, exactly where striate band on sternite VIII (Fig. 39), and modified sensilliform seta P4
psm pores are located in the new species. Furthermore, Tuxen (1964, on metanotum (Fig. 40) (Szeptycki & Weiner 1997; Shrubovych et al.
p. 225) confirmed that these were dermal glands, not setae. 2012, 2014b). Australentulus also has a well-developed striate band,
The genus Acerentuloides belongs to the group of Berberentulinae but differs in possessing reduced labial palpi and 4 setae on sternite
genera sensu Szeptycki (2007) that possess 3 setae on abdominal legs, VIII. Andinentulus, Brasilidia, and Fjellbergella also have 6 setae on
Shrubovych et al.: Molecular phylogeny of Acerentomidae, Acerentuloides bernardi sp. nov. 441
Table 2. Body chaetotaxy of Acerentuloides bernardi Shrubovych sp. nov., 2016.

Dorsal Ventral

Segmenta Formula Setal composition Formula Setal composition

Th I 4 1, 2 4+4 A1, 2, M1, 2
6 P1, 2, 3
Th II 6 A2, 4, M 5+2 Ac, 2, 3, M
16 P1, 1a, 2, 2a, 3, 3a, 4, 5 4 P1, 3
Th III 6 A2, 4, M 7+2 Ac, 2, 3, 4, M
16 P1, 1a, 2, 2a, 3, 3a, 4, 5 4 P1, 3
Abd I 6 A1, 2, 5 3 Ac, 2
10 P1, 2, 2a, 3, 4 4 P1, 1a
Abd II–III 6 A1, 2, 5 3 Ac, 2
14 P1, 2, 2a, 3, 4, 4a, 5 5 Pc, 1a, 2
Abd IV–V 6 A1, 2, 5 3 Ac, 2
14 P1, 2, 2a, 3, 4, 4a, 5 8 P1, 1a, 2, 3
Abd VI 8 A1, 2, 4, 5 3 Ac, 2
14 P1, 2, 2a, 3, 4, 4a, 5 8 P1, 1a, 2, 3
Abd VII 8 A1, 2, 4, 5 3 Ac, 2
16 P1, 1a, 2, 2a, 3, 4, 4a, 5 9 Pc, 1, 1a, 2, 3
Abd VIII 6 A2, 4, 5 4 1, 2
16 P1, 2, 2a, 3, 3a, 4, 4a, 5 2 P1a
Abd IX 12 1, 1a, 2, 2a, 3, 4 4 1, 2
Abd X 12 1, 1a, 2, 2a, 3, 4 4 1, 2
Abd XI 6 1, 3, 4 6
Abd XII 9 6
a
Abd = abdominal segments, Th = thoracic segments.

sternite VIII, but differ from Acerentuloides by having a reduced labial abdominal legs II and III. Additionally, it differs from Najtentulus by the
palpus with 3 setae and a sensillum, and in reduction of the striate shape of the foretarsal sensillum t3 (finger-like in Acerentuloides, cylin-
band to 2 lines without visible striae (Nosek 1973; Shrubovych & Ber- drical in Najtentulus). The presence of a vesicle on the maxillary gland
nard 2013; Shrubovych et al. 2014c). is found in only a few genera (Vesiculentomon Rusek, 1974, Nosekien-
Acerentuloides is morphologically close to the genera Acerentu- tomon (Nosek, 1977), Callientomon Yin, 1980, and Acerella Berlese,
lus and Najtentulus, differing from them by the peculiar shape of the 1909), but they belong to other subfamilies of Acerentomidae (Tuxen
maxillary gland and strong reduction of the subapical median seta on 1964; Shrubovych et al. 2014a).

Figs. 35–40. Acerentulus confinis (Berlese, 1908), American specimen scanning electron microscopy photographs. 35. Habitus; 36. pseudoculus and cephalic setae
sd4 and l3; 37. foretarsus, exterior view: sensilla t1, t3 and a’; 38. labial palpi with apical tuft of setae and basal sensillum (s); 39. sternite VIII; 40. modified seta P4
on metanotum. Scale bars = 300 µm (Fig. 35), 20 µm (Figs. 36 and 38), and 40 µm (Figs. 37, 39, and 40).
442 2017 — Florida Entomologist — Volume 100, No. 2
Phylogenetic analyses, using both parsimony and ML, strongly sup- Within Berberentulinae, species of Acerentulus form a separate
port Acerentomidae as monophyletic (Fig. 41). Monophyly of Aceren- and strongly supported taxon, which is sister group to a clade Andinen-
tomidae was already supported by the analysis of 67 morphological tulus + Baculentulus + Gracilentulus. Within Acerentulus, A. confinis is
characters for 35 species of Acerentomata (Shrubovych 2014). The the sister group of the remaining species of the genus. The Berberen-
topology supports a monophyletic position of Berberentulinae. Ber- tulinae are sister group to a clade comprising all remaining subgroups
berentulinae is a subfamily including many genera (29 genera accord- proposed by Szeptycki (2007), i.e., Acerellinae + Nipponentominae +
ing to Szeptycki 2007) (Shrubovych 2014). In the present analyses, we Acerentominae. Acerentominae are paraphyletic due to the position of
included only 4 species of Berberentulinae, therefore more informa- the Nosekiella (Nipponentominae) as sister group to Huashanentulus
tion about genetic data for morphologically differing genera of Ber- (Acerentominae). François (2003) proposed to create a separate sub-
berentulinae is needed (such as Amphientulus Tuxen, 1981, Australen- family of Huashanentominae for genera Huashanentulus Yin, 1980 and
tulus Tuxen, 1967, Kenyentulus Tuxen, 1961, Silvestridia Bonet, 1942, Sugaentulus Imadaté, 1978 based on 2 apomorphies: absence of fore-
and Tasmanentulus Tuxen, 1984) to clearly confirm monophyly or even tarsal sensillum b’ and well-developed striate band. These characters
discuss family status for subfamily Berberentulinae. also are native for other members of the subfamilies Nipponentomi-

Fig. 41. Molecular phylogeny of Acerentomidae inferred from concatenated COI, 18S rRNA, 28S rDNA D1–D2, and 28S rDNA D3–D6 sequences with maximum
likelihood (ML). ML bootstrap values shown above the branches.
Shrubovych et al.: Molecular phylogeny of Acerentomidae, Acerentuloides bernardi sp. nov. 443
nae, Acerellinae, and Acerentominae sensu Szeptycki (2007). Cladistic Nosek J. 1973. The European Protura. Their Taxonomy, Ecology and Distribu-
analysis, based on morphological characters, shows a separate posi- tion with Keys for Determination. Muséum D’Histoire Naturelle, Genève,
Switzerland.
tion of Huashanentulus and Sugaentulus in a group of Acerellinae + Nosek J, McEwan Kevan DK. 1984. A species of Acerentomidae (Protura) new to
Nipponentominae + Acerentominae genera (François 2003, p. 118, fig. Canada. Revue d’Entomologie du Quèbec 29: 55–61.
2, consensus tree). However, these genera do not form a joint clade on Rambaut A, Drummond A. 2010. FigTree v1.3.1. Institute of Evolutionary Biol-
the consensus tree. Szeptycki (2007) included these genera in Aceren- ogy, University of Edinburg, Edinburg, United Kingdom.
tominae together with morphologically similar genera (Shrubovych & Resch C, Shrubovych J, Bartel D, Szuscich NU, Timelthaler G, Bu Y, Walzl M, Pass
G. 2014. Where taxonomy based on subtle morphological differences is per-
Rusek 2010). The genus Huashanentulus should be included in Nip- fectly mirrored by huge generic distances: DNA barcoding in Protura (Hexa-
ponentominae according to our genetic results due to the strongly poda). PLoS One 9: e90653.
supported joint clade Huashanentulus huashanensis Yin, 1980 with Rusek J, Shrubovych J, Szeptycki A. 2012. Head porotaxy and chaetotaxy of or-
Nosekiella sinensis Bu & Yin, 2008. We need additional genetic data der Acerentomata (Protura). Zootaxa 3262: 54–61.
Schneider C, D’Haese CA. 2013. Morphological and molecular insights on Mega-
for remaining nipponentomine and acerentomine genera to arrive at lothorax. The largest Neelipleona genus revisited (Collembola). Invertebrate
more comprehensive phylogenetic hypotheses. Systematics 27: 317–364.
Shrubovych J. 2014. Identification and character analysis of the Acerentomidae
(Protura) of the northeastern Palearctic (Protura: Acerentomidae). Zootaxa
Acknowledgments 3755: 136–164.
Shrubovych J, Bernard EC. 2013. Review of Tuxenentulus and Fjellbergella spe-
cies (Protura: Acerentomidae, Acerentominae). Annals of the Entomological
We thank the anonymous reviewers for their helpful comments. Society of America 106: 673–683.
We are thankful to K. Tajovský and J. Frouz for collection of proturan Shrubovych J, Rusek J. 2010. Sugaentulus andrzeji sp. nov. from Siberia, Russia
(Protura: Acerentomidae: Acerentominae) and key to Acerentominae gen-
material in the Patoka River National Wildlife Refuge, Indiana, USA, era. Zootaxa 2720: 59–68.
and to E. C. Bernard for collection of A. confinis material in Tennes- Shrubovych J, Schneider C, D’Haese CA. 2012. Description of a new species of
see, USA, and for his correction of English. Field collection (2008) was Acerentulus Berlese, 1908 (Protura: Acerentomata: Acerentomidae) with its
supported by CaFoTrop (www.cafotrop.com). The laboratory work was barcode sequence and a key to the confinis group. Annales de la Société
done in the D’Haese’s BoEM laboratory. This research received support entomologique de France 48: 1–7.
Shrubovych J, Rusek J, Bernard EC. 2014a. Revision of Vesiculentomon,
from the SYNTHESYS Project (http://www.SYNTHESYS. Info/), which is Nosekientomon n. g. (Protura: Acerentomidae, Nipponentominae) with a
financed by European Community Research Infrastructure Action un- key to genera of Nipponentominae. Annals of the Entomological Society of
der the FP7 Integrating Activities Programme and from the Ministry of America 107: 74–80.
Education, Youth, and Sports, project no. ME08019. Shrubovych J, Schneider C, D’Haese CA. 2014b. Two new species of Acerentulus
Berlese, 1908 (Protura: Acerentomata: Acerentomidae) with its barcode se-
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