Two new species of the family Nippobodidae (Acari, Oribatida), including a description of the leg-folding process
Two new species of the family Nippobodidae (Acari, Oribatida), including a description of the leg-folding process
Nestor Fernandez 0
0 National Council of Scientific and Technological Research (CONICET), Evolutive Genetic Laboratory FCEQyN, Misiones National University , Felix de Azara 1552, 6o, 3300 Posadas Misiones , Argentina 2 Research Unit for Environmental Sciences and Management, North-West University , Potchefstroom, 2520 , South Africa 3 National Institute Agricultural Technology (INTA), Experimental Rural Agency , Aimogasta , Argentina
Nippobodes panemorfis sp. n. and Leobodes trypasis sp. n. are described by means of optical and Scanning Electron Microscopy (SEM) and compared to other congeners. The leg-folding process is described and illustrated. Nippobodes panemorfis sp. n. is characterised by interlocking, double hook-shaped, posterior prodorsal condyle and anterior zone humeral apophysis; posterior prodorsal depression present. Tutorium a large lamina defining a pocket-shaped structure; bothridial opening ovoid, situated at the bottom of a U-shaped structure; deep, rounded-ovoid anterior notogastral depression present; ten pairs of notogastral setae; c setae looped, dentate, sharply tipped. Marginal setae h3, p3 on large promontories, followed by deep Vshaped incision; notogaster completely surrounded by circumgastric depression; lateral genital zone with locking structure constituted by longitudinal cuticular elevation, with promontories and a parallel furrow involved in the leg-folding process; genital plate smaller than anal plate. Leobodes trypasis sp. n. is characterised by: the presence of posterior prodorsal depression and anterior notogastral depression; bridge-shaped anterior prodorsal condyles; heart-shaped frontal prodorsal orifice; ten pairs of notogastral setae; posterior prodorsal condyle and humeral condyle interlocked, forming double hook-like structure; circumgastric furrow surrounding entire notogaster; setae lp, h2, h1 situated on shallow medial furrow; notogastral setae lm, lp, h1, h2 medially aligned; p1, p2, p3, h3 marginally situated. Legs I-IV, tutorium, pedotectum I, and pedotectum II involved in leg folding which is inferred to be a protection mechanism.
In 1959 Aoki described the new genus Nippobodes from material collected by Mr. K.
Kaneko in Hiketa-Machi Kagama, south Japan. Aoki compared the genus to
Tetracondyla, but in the same paper, without further explanation, included the new genus
in the family Carabodidae. Nippobodes insolitus
was the first species to be
described, and in 1961 Aoki gave a diagnosis for a new family, Nippobodidae,
incorporating the genus Nippobodes. Other species were later added, such as: Nippobodes
; N. brevisetiger
; N. yuwanensis
; N. monstruosus
Jeleva & Vũ, 1987; N. tokaraensis
; N. chejuensis
; and N.
was the second genus to be added to the family
Nippobodidiae, with Leobodes mirabilis, collected in Mae Ngon Luang, Thailand, as type species.
Other species were subsequently described: L. mirabilis
; L. anulatus
; L. lijiangensis Aoki, 2000; and L. yinae
Three species were collected in China and described as new species of Nippobodes:
N. flagellifer Chen & Wang, 2007; N. peniculatus Chen & Wang, 2007 and N. pseudo
brevisetiger Chen & Wang, 2007. In the same paper the authors added two new species
of Leobodes: L. carinatus Chen & Wang, 2007 and L. praeconcavus Chen & Wang,
2007, transferring Nippobodes monstruosus Jeleva & Vũ, 1987 to the genus Leobodes as:
(Jeleva & Vũ, 1987)
Chen and Wang 2007 proposed a revised diagnosis of the family and provided
a key of species described worldwide. That study was based on adult stages, making
use of optical microscopy and including some digital images. Legs were discussed in a
fragmentary fashion but detailed elements were not included in previous studies and
the leg-folding process was not mentioned.
More than five years ago, the current authors embarked on a revision of the
Carabodidae family. During these studies, we observed a series of similar characters in
Carabodidae and Nippobodidae not discussed in previous studies of Nippobodidae.
Aspects such as the leg-folding process, discussed by Fernandez et al. with reference to
the Carabodidae family
(Fernandez et al. 2013a)
, are also present in Nippobodidae,
with some similarities and significant differences.
Difficulties were encountered in our efforts to provide detailed comparisons with
previous papers, mainly due to simplified drawings and descriptions. Frontal and
lateral views are often lacking, making it difficult to determine if some structures are
absent in previously described species, or if they were not mentioned by authors. We
explain the leg-folding process by use of illustrations, complementing the study with
SEM micrographs, and include a comparison of the two families.
Two new species of the family Nippobodidae (Acari, Oribatida), including a description... 111
Materials and methods
Specimens studied by means of light microscopy followed the techniques described
Krantz and Walter 2009
. Specimens studied under SEM,
followed the techniques of
Alberti and Fernandez 1990
a, 1990b; Alberti et al. 1991,
Fernandez et al. 1991
. Equipment used was the same as for previous
(see Fernandez et al. 2016)
Optical drawings should be considered semi-schematic with regard to cuticular
microsculpture and setal shape. The shape of these specimens made it difficult to
orientate the material and obtain the same position consecutively. Studies with SEM
provided high levels of precision and detailed Figures; another very important aspect was
the positioning system, permitting orientation of material with a much higher level of
precision, as well as being able to return to an initial position.
Body measurements taken: total length (from tip of rostrum to posterior edge
of notogaster); width (widest part of notogaster). Setal measurements taken on three
specimens under SEM. Leg chaetotaxy studies used optical microscopy (standard,
polarised, and phase contrast) and SEM.
Setal formulae of legs include the number of solenidia (in parentheses); tarsal setal
formulae include the famulus (ε). All measurements are given in micrometres (μm).
Morphological terms and abbreviations used are those developed by Grandjean
Travé and Vachon 1975
Norton and Behan-Pelletier 2009
; 1961; 1965a; 1965b; 1989; Fernandez et al. 2013; 2013 a, b, c; 2014; Chen
and Wang 2007. For setal types Evans (1992: 73) and for ornamentation of cuticular
surfaces Murley (1951) were used. Additional terms and abbreviations are given below.
MNHG Museum of Natural History, Geneva, Switzerland.
a.o frontal prodorsal orifice
a.pr.b bridge-shaped anterior prodorsal condyles
la.le lateral ledge
m.f medial shallow furrow
p.pr.co posterior prodorsal condyle
New taxon descriptions
Nippobodes panemorfis sp. n.
Etymology. The specific epithet “panemorfis” is derived from “panemorfi” (πανεμορφη
in Greek) meaning beautiful, due to the aesthetic features of the cuticle and setae.
Diagnosis (adult female). Prodorsum. Complex shape; triangular in dorsal view
with rounded central posterior zone; double hook-shaped, interlocking posterior
prodorsal condyle and anterior zone humeral apophysis; rounded rostrum, with groove
and large hump; deep, easily discernible round-ovoid prodorsal posterior depression;
tutorium strongly curved, large lamina, connected to prodorsal wall, determining a
pocket structure. Reticulate-foveate microsculpture on tutorium, pedotectum I,
pedotectum II. Polyhedral bothridium situated under zone where humeral part, overlaps
with anterior prodorsal zone; bothridial opening ovoid, located at bottom of U-shaped
structure. Notogaster: deep, round-ovoid anterior notogastral depression present; ten
pairs of setae c, la, lm, lp, h1, h2, h3, p1, p2, p3; setae c looped, dentate, sharply tipped;
marginal setae h3, p3 on conspicuous promontories, followed by deep v-shaped
incision; circumgastric depression completely surrounding notogaster, originating before
setae la, running between setae la, h1, h2 and h3, p3, p2, p1; setae 1c, 3c, 4b situated
marginally; setae 1b largest; genital opening on elevated zone; lateral genital zone
locking structure with, longitudinal cuticular elevation, promontories with parallel furrow;
genital plate smaller than anal plate; adanal setae ad1, ad2 inserted on elevated zone;
ad3 setae smallest.
Material examined. Holotype: ♀♀ Female. Label details: “Thailande. Khao
Yai National Park (nord-est de Bangkok) Khao Khieo au-dessous d’Air Force check
point; 1150 m; versant nord, forêt assez sèche; tamisage débris. 28/XI/1985. Leg:
D.H. Burckhardt et L. Löbl”. Paratypes: Two adult females, same locality and date
as Holotype; deposited in Collection of NHMG; preserved in 70 % ethanol.
Additional material studied using SEM: six specimens, not deposited. “Thailande. Khao
Yai National Park (nord-est de Bangkok) Khao Khieo au-dessous d’Air Force check
point; 1150 m; versant nord, forêt assez sèche; tamisage débris. 28/XI/1985. Leg: D.H.
Burckhardt et L. Löbl”
Description. Measurements. SEM: 597 (542–720) × 368 (332–401) (n = 6). Light
microscopy: 610 × 360 (n = 1); all specimens female. Shape. Rounded-ovoid (dorsal
view) (Figure 1). Elongate oval (lateral view) (Figures 11, 23).
Colour. Black, slightly shiny when observed in reflected light; rarely dark brown.
Cerotegument. Not observed; small particles, similar to rest of cerotegumental layer
on circumgastric depression (s.c) lateral zone (Figure 16); the layer may have existed.
Integument. Microsculpture complex, varying according to body region. Smooth:
prodorsum (on Figure 4 indicated by T); notogaster (on Figures 1, 7 indicated by T); on
most epimeral surface (on Figures 28, 41 indicated by T); genital, anal, aggenital zones.
Tuberculate: rostum (Figure 14, indicated by z); infracapitulum near setae h (Figure 42,
indicated by z); epimeral zone between setae 1a, 1b (Figure 28, indicated by z).
Reticulate-foveate: Tutorium (Tu) (on Figure 26 indicated by v); Pedotectum I (Pd I)
(on Figures 26, 27 indicated by v), Pedotectum II (Pd II) (Figure 20, indicated by v).
Rugose: external zone of humeral apophyse (h.ap). (Figures 1, 4, 7, 8, 9, 23, indicated by
R). Favulariate: bothridial zone (Figure 24a, indicated by *). Sulcate: zone of bothridial
opening (Figure 24a, b indicated by ¡). Punctate: Discidium (dis) (Figure 30 indicated
by ¿); epimeral zone surrounding setal insertion (Figures 30, 43, indicated by ¿).
Two new species of the family Nippobodidae (Acari, Oribatida), including a description... 113
Prodorsum. Complex shape: in dorsal view, more or less triangular with central
posterior zone rounded (Figures 1, 4); lateral posterior zone with interlocking double
hook-shaped posterior prodorsal condyle (p.pr.co) (indicated by ◙) and anterior zone
humeral apophysis (h.ap) (Figures 8, 9); lateral view: triangular; with complex lateral
posterior zone, with double hook and sigmoid lamellae (Figure 23).
Rostrum round, with a conspicuous groove parallel to margin (Figure 23 indicated
by ¿) large hump visible in front of groove (Figures 14).
Setae: sigmoid, with small dentitions and thin parallel longitudinal ridges: Rostral
(ro), interlamellar (in), lamellar (le) setae (Figures 1, 4, 5, 6, 9,10, 21, 22): length:
123 (106–141) (n = 12); setae le, in , inserted each on large tubercle, setae ro inserted
on small tubercle (Figures 1, 4, 9, 26); setae ro situated behind region of
tuberculate microsculpture, marginally to depression created by Tu and lateral prodorsal wall
(Figures 4, 26); le setae inserted on anterior end of lamellar zone (Figure 26), situated
posteriorly and to the exterior of ro setal insertion alignment (Figures 1, 4, 7); setae in
situated behind and externally to le setal insertion level (Figures 1, 4, 7), inserted near
the double hook (Figures 8, 9); deep, rounded-ovoid prodorsal posterior depression
(p.p.d) clearly discernible between dorsosejugal furrow (d.sj) and notogastral anterior
depression (n.a.d) (Figure 1).
Lamellae (Lam) clearly visible in lateral view (Figures 11, 23) (see Lateral Region).
Bothridium (bo) (Figures 23, 24) situated under double hook zone (See: Lateral view).
Sensillus (si) (Figures 17, 18) sickle-shaped, strongly curved, directing upward with
long stalk followed by a swollen zone, plentifully scattered with small asperities and
with small barbs (Figure 18 indicated by ¡); long sharp apical tip; length 152 (149–
160) (n = 6). Tu well developed, sharply tipped; lacking free extremity, welded to
lateral prodorsal wall, determining pocket-like structure (Figures 4, 26). Pocket structure
conceals leg I when leg-folding process is activated (See: Leg-Folding Process).
Interlocking double hook. The interlocking double-hook zone is complex, formed
by p.pr.co and anterior zone h.ap (Figures 1, 4, 7, 8, 9, 23); where h.ap situated
externally (indicated by *), grips on to p.pr.co (indicated by ◙) on the interior. Cuticular
surface of p.pr.co smooth with some irregular depressions (Figure 8); cuticular surface
of h.ap rugose externally (Figures 1, 4, 7, 8, 9 indicated by R), internally smooth.
Notogaster. Dorsal view, notogaster polyhedral-rectangular shape (Figure 9); d.sj)
convex, clearly delimited (Figure 1). Deep, round-ovoid n.a.d present, extending
posteriorly from d.sj.
Ten pairs of setae c, la, lm, lp, h1, h2, h3, p1, p2, p3; setae c situated on lateral margin
of n.a.d (Figures 1, 4, 7); setae c: looped, dentate, sharply tipped (Figure 19). Length:
150 (144–175); la, lm, lp, h1, h2, h3, p1, p2, p3 (Figures 1, 2, 16, 23, 25): simple, small
dentitions, with parallel longitudinal ridges, sharply tipped (Figure 3); four pairs situated
laterally: h3, p1, p2, p3; three pairs (la, h2, h1) situated internally to s.c; two pairs (lm,
lp) situated internally to la, h2 (Figures 1,7, 23). Setae h3, p3 inserted on conspicuous
promontories (Figure 1, 23, 25, 42); deep v shaped incision observed behind each seta
(Figure, 25, indicated by ¿), determining a scalloped notogastral margin in this region
(Figure 1). Setal lengths: la 102 (97–112); lm 134 (127–142); lp 125 (118–132); h1, h2
70 (68–76); h3 91 (86–98); p3 59 (56–64); p2, p1 43 (41–47); s.c completely
surrounding notogaster, originating slightly in front of setae la, running between setae la, h1, h2
and h3, p3, p2, p1 (Figures 1, 7 trajectory indicated by l).
Posterior notogastral view (Figure 7). Deep ovoid p.p.d as well as n.a.d clearly
visible; setae c situated on paraxial zone of h.ap.
Trajectory of s.c indicated by l; externally to s.c, flat surface of notogaster
extending from s.c to notogastral margin; scalloped zone (behind setae h3, p3), some distance
from s.c, not interrupting its trajectory.
Lateral region. Tu strong, large lamina, together with prodorsal wall and
lamellae determining a pocket structure; anterior Tu ending in sharp angle, with interior
part welded to prodorsal wall (Figure 1 indicated by 6); behind le setal insertion level,
pocket structure internally delimited by the Lam (Figures 23, 26) (See Leg-folding
process). Pd I, prominent extended lamina; (Figures 26, 27). Pd II, small lamina, rounded
apex (Figures 20, 23); Tu, Pd I, Pd II with reticulate-foveate cuticular microsculpture
(Figures 20, 26, 27 indicated by v).
Complex, polyhedral bo situated under the zone where h.ap overlaps the
anterior prodorsal zone (Figure 23). Bothridial opening observed at the bottom of a long
U-shaped structure (Figures 24a, 24b), with sulcate microsculpture on inferior zone
(Figure 24a, 24b indicated by ¡); smooth bothridial ring (bo.ri) surrounding ovoid
botridial opening; Lam sigmoid, lacking sharp cuspis (Figures 23, 26); setae le inserted
on promontories at Lam apical zone; s.c clearly visible, originating in zone anterior to
la setal insertion level (Figure 23, trajectory indicated by l); v-shaped incision
observed behind h3, p3 setae (Figure 25, indicated by ¿); b.ng convex (Figure 23).
Ventral region. Epimeral chaetotaxy 3–1–3–2 (Figures 13, 42); setae 1c, 3c, 4b
situated marginally (Figure 30); setae 1b largest (Figure 41); epimeral borders easily observed;
bo.2, b.sj traversing medial plane; bo.3 small; apodemes apo.1, apo.2, apo.dj, apo.3 clearly
visible (Figure 13); small setae, many small barbs (Figure 30); length: 9 (5–18).
Genital plate ovoid, with four pairs of setae (Figure 35, 36, 37); genital setae: with
small barbs, variable in shape (Figures 36, 37); length: 5 (4–7); genital opening on
elevated zone (Figures 28, 35); setae ag in margin of elevated zone (Figures 28, 32, 42);
medium sized setae ag with small dentitions, sharp tip (Figures 32) ag: 20 (8–21).
Complex structure involved in leg-folding process (see Locking structure), situated laterally to
setae ag (Figures 28, 31, 42); constituted by longitudinal cuticular elevation, with parallel
furrow and lateral to it a cuticular promontory and opposite, a polyhedral plate (in
Figures 28, 42 indicated by S) (see Leg-folding process); genital plate smaller than anal plate
(Figures 28, 42). Anal opening with elevated zone posterior to h3 insertion level (well
visible in ventral posterior view) (Figure 42); anal plate more or less rectangular with
rounded anterior and posterior zones; two pairs of anal setae (Figures 28, 32, 38, 42).
Setae: an small dentitions, parallel ridges (Figure 39), length 14 (15–20); three pairs
of adanal setae (Figures 28, 33, 38, 42); setae ad1, ad2 inserted on elevated zone; ad3 setae
smallest (Figures 38, 42); adanal setae: medium sized, small dentitions, sharply tipped
(Figures 32, 33), length 32 (30–36). Three pairs of subcapitular setae, h, m and a: h, m
simple, finely barbate (Figures 34a, 44), a elongated leaf-shaped, with some narrow, shallow
longitudinal furrows (Figure 34b); setae h situated in margin of tuberculate zone (Figure
42 indicated by z); setae m curving, lengths: h 10 (9–12); m 30 (28–32); a 11 (10–12).
Palp (Figure 34): the first four segments display normal setation (0–2–1–3); tarsus
particular, presenting only: cm barbate, (vt) barbate, w solenidion and eupathid acmx,
sulx, ul’x, ul”x. Solenidion unusually shaped (Figures 45, 46), with porous surface (Figure
47); eupathid sulx, ul’x, ul”x with an obvious apical perforation (Figure 46).
Legs. See Figures 48–53, Table 1. All legs with very small genu and long tibia.
Femur leg IV with large round porose area (Figure 53). Femur III with large femoral
groove (f.g) (Figures 51, 52) (see Leg-folding process). Setal formulae I (1–4–2–4–16–
1) (1–2–2); II (1–4–3–2–15–1) (1–1–2); III (2–3–1–2–15–1) (0–1–0); IV (1–2–1–
Remarks. Future ontogenetic studies are necessary in order to confirm
nomination of notogastral setae. As only the adult stase was available for study, we used
standard, previously used notation (see Morphological terminology). We were unable to
locate information on the palp in previous studies. Setae l’ of genu II were indicated
Chen and Wang (2007)
as bifurcate; however, in our studies only one instance of
bifurcate setae l’ was observed. Another particularity is the presence of (it) on tarsus IV.
The femoral groove was observed, though not indicated in any previous study.
Leobodes trypasis sp. n.
Etymology. The specific epithet “trypasis” is derived from τρύπα in Greek meaning a
hole, due to the characteristics of the anterior prodorsum.
Diagnosis. Rostrum ovoid; smooth cuticula with isolated verrucous tubercles; setae
ro sigmoid; setae le curved, directing forward and upward; setae in slightly sigmoid,
Two new species of the family Nippobodidae (Acari, Oribatida), including a description... 123
ing forward; deep round-ovoid posterior prodorsal depression; massive posterior prodorsal
condyles, posterolaterally located, extending anteromedially to form a curved bridge,
interlocking medially in undulate zone. Lateral lamellae, curved ribbon; frontal orifice, heart
shaped; translamella curved; tutorium welded to lateral prodorsal wall, determining
pocket structure, sharply tipped, but welded to lateral prodorsal wall; sensillus sickle-shaped,
strongly curved, upwards; long stalk, swollen middle zone, apically long sharp end.
Anterior notogastral depression deep, ovoid-elongate shape; humeral apophysis overlapping
posterior prodorsal condyle, extending to the proximity of interlamellar setae;
circumgastric depression, surrounding whole entire notogaster; setae c hook-shaped; flat smooth
surface surrounding laterally whole notogaster; flat, smooth lateral ledge, surrounding entire
notogaster; anterior zone, ribbon shaped; genital plate smaller than anal plate.
Material examined. Holotype: ♀ Female “VN 12/03c Vietnam. Vinh Phuc Prov.
evergreen Forest 1 km SE Tam Dao city. 21°26'49"N, 105° 39'06"E. 13/14/V/2012.
Leg. P. Schwendinger & A. Schulz”.
Description. Measurements. SEM: 680 (610–750) × 336 (302–400) (n = 5).
Light microscopy: 701 × 341 (n = 1); all specimens female.
Shape. Oval (Figure 54).
Colour. Dark brown to black; slightly shiny when observed in reflected light.
Cerotegument. Not present.
Integument. Microsculpture varying according to body region: Smooth: p.pr.co
interior zone; transversal bridge-shaped structure (a.pr.b) (Figures 54, 55, 58); superior
Lam zone; superior and apical region Tu (on Figures 56, 65 indicated by T).
Notogaster: central zone; marginal zone between s.c and b.ng (on Figure 62 indicated by T);
flat lateral ledge (la.le) situated immediately above b.ng (see below) (on Figures 62, 63
indicated by T); epimeral zone (on Figures 71, 72 indicated by T); infracapitulum (on
Figure 71 indicated by T). Tuberculate (two types). Small tubercles: prodorsal zone below
frontal orifice (a.o) and between setae le (on Figure 56 indicated by X); large verrucous
tubercles (Figure 70): isolated tubercles, dispersed on prodorsum (Figures 56 indicated
by *), notogaster (Figure 55, indicated by *), and ventral zone (Figure 62, indicated by
*). Rugose: external zone h.ap, external zone of pr.co (Figures 54, 55, 56, 58 indicated
by R). Reticulate-foveate: basal zone of Lam, (Figure 62, indicated by v); Tu (Figure
62, indicated by v); Pd I anterior zone. Sulcate: area of bothridial opening (Figure 64,
indicated by ¡).
Setation (legs not included). Simple, smooth: subcapitular setae a. Simple, small,
dentate, parallel longitudinal ridges (Figure 66): prodorsal (Figures 67, 68), notogastral
(Figure 57, 69), epimeral, subcapitular m, h; genital, aggenital, adanal, and anal setae.
Prodorsum. More or less triangular in dorsal view, central posterior concave;
lateral view: polyhedral (Figure 62); lateral posterior zone with double hook, interlocking
posterior prodorsal condyle (p.pr.co) and h.ap anterior zone (Figures 54, 55). Rostrum
ovoid. Smooth cuticula with some isolate verrucous tubercles (Figures 56, 58) on zone
delimited by rostrum and ro setal insertion level. Setae ro, le, in inserted each on large
tubercle; ro sigmoid, directing forward (Figure 67), length 150 (142–161) (n = 10);
le setae curved, directing forward and upward, length: 106 (102–112) (n = 10),
situated on apical lamellar zone (Figures 56, 68); setae in length: 178 (172–190) (n = 10);
slightly sigmoid, directing forward, situated externally, anterior to h.ap (which overlaps
with posterior prodorsal zone) and posterior to rugose lateral zone of p.pr.co
(Figures 56); p.p.d clearly discernible, deep, round-ovoid in shape (Figure 54, 55, 56, 58).
Massive p.pr.co, hook-shaped, located posterolaterally; anteromedially curved bridge
(a.pr.b), interlocking medially in an undulate zone (Figures 54, 55, 56, 58).
Lamellae (Lam) clearly visible; lateral longitudinal rib, dorsally concave (Figure
56, 57). Conspicuous heart-shaped a.o (Figures 56, 58), located below the a.pr.b, and
between setae le, limited inferiorly by Translamella (trl); trl. a curved structure, running
parallel to and below a. o (Figure 56). Tu well developed; welded to lateral prodorsal
wall, determining a pocket (Figures 56 indicated by ¿); large sharp tip (Figures 54, 58
indicated by 5). Bo complex (Figures 62, 64), situated under la.le (see: Lateral region).
Si (Figure 64) sickle-shaped, strongly curved, directing upward with long stalk,
followed by swollen zone, long sharp apical tip; plentiful small asperities and small barbs
on swollen zone (Figure 64); length: 150 (146–161) (n = 12).
Notogaster. Deep, elongate ovoid n.a.d present, extending from posterior to more
or less half of total notogastral length; medial posterior n.a.d zone, open without
Two new species of the family Nippobodidae (Acari, Oribatida), including a description... 129
ly defined margin; n.a.d lateral marginal zone with three lines; more externally: a short,
concave line on interior of h.ap margin; rectilinear central line; third line lateral to
posterior margin (Figure 54). Anterior h.ap zone overlapping p.pr.co (double hook),
extending to the proximity of setae in (Figures 54, 56); s.c completely surrounding the
notogaster; originating at level of la setal insertion, running internally to setae h3, p3,
p2, p1 (Figures 54, 55, 62 trajectory indicated by l).
Ten pairs of setae: c, la, lm, lp, h1, h2, h3, p1, p2, p3 (Figures 60, 62); setae c
hookshaped (Figure 69), situated on lateral margin of n.a.d (Figures 54, 55, 56); four pairs
situated marginally: p1, p2, p3, h3; four, more or less aligned pairs lm, lp, h2, h1, situated
internally (Figure 55); lp, h2,h1 on medial shallow furrow (m.f); only clearly discernible
in dorsoposterior view (on Figure 55 indicated by v); setae la situated between h3,
p1, p2, p3 and lm, lp, h2, h1 (Figures 54, 55 ). Setal lengths. c: 167 (156–172); la: 100
(83–102); lm: 75 (72–81); lp: 83 (81–89); h3: 125 (123–131); h2:145 (93–147); h1:
154 (101–162); p3: 125 (100–132); p2: 145 (116–137); p1: 73 (71–78).
Lateral region. The tutorium (Tu) strong, large lamina, attached to prodorsal wall,
determining a pocket structure; terminating anteriorly in long sharp tip (Figure 65);
the welded zone of Tu is U-shaped, and the claw of leg I is extended outwards during
the leg-folding process (Figure 56) (see Leg-folding process).
Lamella (Lam) forming conspicuous curved ribbon (Figure 56, 59); running more
or less parallel to Tu margin; setae le situated on promontories on apical zone. Pd
I: prominent lamina, directing forward, slightly tilted down. Pd II a small lamina,
rounded apex; on basal zone a small hump directing outwards (Figure 62). The area
immediately above b.ng is flat, smooth, surrounding the entire notogaster (Figure 62,
trajectory indicated by 6); this flat surface, forms a prominent la.le, parallel to h.ap
(Figure 62); la.le anterior zone, ribbon shaped, (Figure 59, 62, 63); b.ng slightly
convex (Figure 62).
Bo complex: polyhedral, situated below la.le (Figure 64); bothridial opening
situated at the bottom of a long U-shaped structure; inferior zone with sulcate microsculpture
(Figure 64), indicated by ¡); bothridial opening ovoid, surrounded by smooth bo.ri; s.c
clearly visible, originating at level of la insertion setal level (Figure 62 indicated by l).
Ventral zone. Epimeral chaetotaxy 3-1-3-2 (Figures 61, 71, 72); setae 1c, 3c, 4b
situated marginally; setal lengths: 1a: 35 (32–38); 1b: 35 (30–37); 1c: 29 (25–31); 2a:
12 (10–15); 3a: 22.5 (20–25); 3b: 38 (35–42); 3c: 18 (16–19); 4a: 50 (45–52); 4b: 38
(41–45); epimeral borders clearly visible; bo.sj crossing transverse medial plane (Figure
72); bo.3 small; apodemes apo.1, apo.2, apo.dj, apo.3 clearly visible (Figure 61). Pd I,
Pd II clearly discernible (Figures 71, 72).
Genital aperture rectangular, anterior margin rounded, four pairs of setae: g1: 71
(68–73); g2 : 49 (44–52); g3: 37 (34–43); g4: 35 (31–38); Elevated ridge surrounding
genital opening medially and towards posterior zone (Figure 72, indicated by *), in posterior
zone a small vertical column present (Figure 71, 72 indicated by 5); setae ag distanced
from genital opening (Figures 71, 72); length: 73 (71–83). Posterior limit epimere IV,
oblique lineal ridge laterally directed (Figure 71, 72 indicated by ¿); originating in
anterior zone of genital plate (Figures 71, 72 indicated by ¿). Complex structure lateral to
setae ag, with a longitudinal cuticular elevation, parallel furrow and promontories (see leg
folding “locking structure”); genital plate smaller than anal plate (Figures 71, 72).
Anal aperture more or less rectangular with rounded anterior and posterior zones;
two pairs of anal setae (Figures 61, 71, 72), length: 37 (35–39); three pairs of adanal
setae: ad1: 73 (71–75); ad2: 75 (73–78); ad3: 80 (77–83). Three pairs of subcapitular
setae: h, m simple, barbate; a simple, smooth: lengths: a: 12 (9–15); m: 29 (28–33);
h: 42 (39–45).
Legs (Figures 73-76, Table 2). Very small genua and long tibia in all legs. Femur
III with f.g (Figure 75) (see Leg-folding process). Setal formulae: I (1-4-2-4-16-1)
(12-2); II (1-4-3-2-15-1) (1-1-2); III (2-3-1-2-15-1) (0-1-0); IV (1-2-1-2-14-1) (0-1-0).
Aoki, when establishing the new genus Nippobodes in 1959, initially included it in the
family Carabodidae. Almost sixty years later, we propose that the family
Nippobodidae presents a series of characters linking these families, as knowledge of the families
Nippobodidae and Carabodidae has grown significantly in the intervening years. We
consider here only some elements that indicate important similarities: 1) prodorsal
posterior depression and notogastral anterior depression situated either side of d.sj; 2)
the projection of h.ap overlapping the posterior area of prodorsum; 3) the structures
involved in leg folding such as tutorium, pedotectum I, genu (functioning as a hinge),
femoral groove in femur III, shapes of femurs. These three elements are insufficient for
a comparison, but highlight some aspects indicating a possible relationship between
the families. More detailed analysis is required, but hampered by the lack of immature
specimens of Nippobodidae and for the greater part of Carabodidae.
Unfortunately descriptions of genera in the family Nippobodidae are often
superficial, and in many instances the frontal and posterior views were neglected although
Two new species of the family Nippobodidae (Acari, Oribatida), including a description... 131
they could potentially provide important information. Leg chaetotaxy is problematic
and we endeavour to obtain new material in order to study legs in a larger number of
specimens. Much of our study material was collected many years ago, and does not
permit detailed study, resulting in leg chaetotaxy necessarily being considered provisional.
It has been difficult to find a species related to Nippobodes panemorfis sp. n. due
to its particular characteristics. Nippobodes flagellifer Chen & Wang, 2007 displays the
most characters in common, as both species present similar disposition of: setae ro on
tubercle near lateral margin of prodorsum; setae le inserted on tubercle on anterior on
lamella; sensillus curved, sickle-shaped, swollen medially; posterior prodorsal condyles
interlocking with notogastral humeral apophyse (but dissimilar in shape). Notogastral
surface smooth; ten pairs of notogastral setae.
The taxonomy of Leobodes trypasis sp. n. is complex. The species is difficult to
compare to other congeners due to their dissimilarity, and the often simplified original
descriptions impede adequate comparison. However, there are similarities to L.
, such as the presence of a heart-shaped prodorsal orifice, but occurring
in a dorsal and not frontal position as in L. trypasis.
Leg-folding process (Figures 77–88)
Fernandez et al. (2013a) have studied the folding of legs as a part of the protection
mechanism in various genera of the family Carabodidae. We were fortunate to have the
opportunity to examine this process in vivo on adults of Carabodes sp. under light microscopy
and document the different steps. Additionally, material was available for SEM-studies,
facilitating comparison with other SEM images. For this paper we were unable to conduct
in vivo studies of the leg-folding process, but based on a series of observed morphological
characteristics and a large number of SEM observations, we do not doubt the presence of
similar functions and processes as observed in genera of the family Carabodidae.
Some morphological characteristics, however, suggest some variation in aspects of
To understand this process one needs, first of all, to embark on detailed studies of
leg structures in Nippobodes (Figures 48–53) and Leobodes (Figures 73–76), as well as
other body structures related to leg positioning. Due to the high number of images
obtained from more than fifty specimens, selected from a total of more than three
hundred animals, only the most representative images of this mechanism have been
included for the sake of clarity.
The following is generally observed: tibia-tarsal articulation by means of a small
section of synarthrodial membrane, allowing limited movement. Tibia and tarsus are long
and narrow, facilitating positioning either in a pocket-shaped structure delimited by
the tutorium (See below), or behind pedotectum I, femur III, and IV (Figures 77–88).
Particular characteristics present in superior part of femur I, allows for partial
concealment under the lateral prodorsal zone, in front of the bothridial zone (Figure 82).
Femur II presents a slightly curved, smooth posterior surface (Figure 83), coapting
with the posterior area of femur III. These structures and surfaces of femurs III and IV
permit perfect coaptation, to allow tibia and tarsus to slip in behind and be concealed
by them (Figures 82, 87).
Leg III plays a vital role. The femoral groove on femur III is a rather deep, triangular
to ovoid groove, with a small seta near the depression. The groove and seta permit
strong, large lamina, anterior zone ending
in sharp angle, with interior part welded to
looped, dentate, sharply tipped
Nippobodes flagellifer Chen & Wang, 2007
rostrum protruding dorsally
large rectangular h.ap interlocking with
posterior part of p.pr.co, triangular to polyedral
(Fig. 18 Chen and Wang 2007)
well developed, large lamina, blunt tip (Fig. 20
Chen and Wang 2007)
proximal half directing anteromedially, distal
half curving posterolaterally
Neither promontories nor incision observed
(Chen and Wang 2007: Fig.18)
inserted on conspicuous promontories;
v-shaped incision behind setal insertion
completely surrounding notogaster;
originating slightly in front of la setae, running hst2aarntsdbpe1h,ipn2d,ph33(iCnhseerntioannd,rWunannign2g0b0e7tw:Feeign.1h81,)
between la, h1, h2 and h3, p3, p2, p1
choring of femur IV into the groove. Femora III and IV each presents a ventral carina,
permitting the tibia and tarsus to be concealed under them (Figures 75, 76, 82, 84).
The tiny genu plays a fundamental role as hinge, and generally presents a reduced
number of setae (Figures 48–53; 73–76). The particular shape of the anterior zone
of the femur improves the genu-hinge function and assists in the tibia-tarsus in the
The tutorium plays a very particular role, forming a pocket-shaped structure with the
lateral prodorsal zone, permitting concealment of tibia-tarsus I. The pocket shaped
structure ends in a sharp point, which protects the leg, and houses the claw (Figures
56, 57). Pedotectum I conceals the tibia and tarsus of leg II.
Lateral zone of body
The lateral area of body is adapted to receive the legs, with depressions and smooth
areas to facilitate their positioning, along with tutorium, pedotectum I, and between
legs II, III, and IV.
The “locking structure”
Ventrally, behind leg IV, a locking structure is observed. It consists of a longitudinal furrow
(on Figures 42, 62, 80, 88, trajectory indicated by l), ending in a bean-shaped structure
(on Figures 42, 80, 87, 88 indicated by v), with a lateral promontory (Figures 42, 88,
indicated by S). Tibia-tarsus IV is inserted into the longitudinal furrow (Figure 80) and the
claw positioned in the depression of the bean-shaped structure (Figures 80, 87, 88). The
femur resembles a lid closing a box, preventing the tibia-tarsus from moving and
anchoring the entire leg in one position (Figure 81, 82, 88).
Phase 1 (Figure 77): Initial position prior to leg folding, arrows indicating the
directions in which legs will move.
Phase 2 (Figure 78): Leg I: femur moves backwards and approaches bothridial
zone; this movement is facilitated by the genu functioning as a hinge. By rotating, it
permits the tibia and tarsus to approach the margin of tutorium. Then, the tibia and
tarsus are positioned ready to initiate installation into the tutorium pocket. Leg II:
the femur moves upward and backward, approaching the posterior zone of femur III;
the tibia and tarsus approach the margin of pedotectum I and move downwards, to
conceal those two segments behind pedotectum I. Leg III: rotates towards the
posterior and femur III moves closer to femur II. The tibia and tarsus slide in under ventral
trochanteric-femoral carinas for concealment. Leg IV: the femur is directed backwards
in order to locate the femoral groove and settle into it. The tibia and tarsus move back
to settle into the longitudinal depression indicated by l (Figure 80).
Phase 3 (Figure 79): Leg I. Femur I approaches the final position on the bothridial
zone; the tarsus and tibia are almost completely concealed behind the tutorium and
embedded in the pocket tutorial depression. Leg II. Femur is coapted to the posterior zone
of femur III. The tibia and tarsus are almost completely hidden behind pedotectum I.
Legs III and IV are very close to each other; femur IV is almost entirely within the
femoral groove of femur III. Tibia and tarsus IV are installed in the longitudinal depression
of the locking structure and tibia and tarsus III slide in and are concealed under femoral
and trochanteral carinae; the claw is visible between trochanters III and IV.
Phase 4, the final position (Figure 81). Leg I: apical dorsal area of femur positioned
under the anterior part of bothridium (indicated by 3 ). The genu rotates inwards
and its dorsal part, as well as the tibia and the tarsus are concealed deep in the tutorial
pocket depression. Leg II. The genu turns inwards to position the tibia and tarsus in
the optimal position; the tibia is slightly curved. With slight rotation of the genu, the
tibia is similar in shape to pedotectum I; the tibio-tarsus articulation gives important
rigidity. The tibia and tarsus descend and are perfectly concealed behind pedotectum I.
Leg III. The posterior zone of femur II glides underneath the anterior part of femur III.
Tibia and tarsus III slide in under the carina of trochanter–femur III for concealment,
and the tarsal claw is visible between trochanters III and IV. Leg IV: the posterior part
of femur IV is placed inside the femoral groove of femur III. Femur IV is inclined
upwards to enable the tibia and tarsus to glide in underneath the femur, and tibia and
Two new species of the family Nippobodidae (Acari, Oribatida), including a description... 137
tarsus IV are placed into the longitudinal furrow of the locking structure. To conclude
the mechanism, femur IV acts as a lid, blocking this segment and concealing the leg
segments in the longitudinal depression, with the claw placed in a horizontal position
resting on the bean-shaped structure of the locking structure (Figure 80).
During the final stages of the coaptation process, the relationship between the legs
and body depressions can be described as follows: tibia and tarsus IV are located in the
longitudinal furrow (of the locking structure), concealed by the femur; the posterior
part of femur IV anchors in the groove of femur III; the apical distal expansion of
femora III and IV partially conceal the genu; apical zone of tarsus III is situated between
trochanter III and trochanter IV (Figures 79, 81). The f.g allows the posterior part of
femur IV to fold into femur III.
Supplementary SEM images
In Figure 82 the final position has almost been reached, with an indication of
structures involved, and arrows indicating the final movement to conclude the process.
Figure 83 indicates the step where femur II is directed to the anterior part of femur III.
The surfaces of the femurs about to come into contact can clearly be seen to fit together
perfectly, and other structures such as the setae are located in such a way that they
do not impede this process. On the posterior zone of Femur III, the femoral groove
shows the seta v, which will assist in anchoring femur IV inside the depression. Figure
84 shows the displacement of femur IV towards the femoral groove (femur III). The
carina of the trochanter and femur is clearly visible, which will permit the tarsus and
tibia of leg III and leg IV to be partially concealed. Figure 85 posterior view, indicates
the final position of legs I, II. The arrows indicate the position of tibia and tarsus I and
II, concealed behind the pedotectum I and tutorium. Figure 86 Shows the lateral view
of final position of legs I and II. Figure 87, posterior view. Tarsus III and tarsus IV are
clearly visible, as well as the claw of tarsus IV and the bean-shaped structure of the
locking structure supporting claw IV. Figure 88 shows theset of fundamental elements
of legs III and IV, as well as cuticular surfaces necessary for the leg-folding process.
Similarities and differences in leg folding between Carabodidae and Nippobodidae
The system is very similar in the two families, and importantly, the following are
common to both: all legs are involved in the process; the presence of the femoral
groove on femur III; a tiny genu, which plays the role of a hinge; the involvement of
pedotecum I and tutorium to conceal legs I and II.
Differences: 1) In Nippobodidae leg I is concealed in a pocket structure formed by
the attachment of the tutorium to the lateral wall of the prodorsum. This connection
to the prodorsal body wall resulting in the formation of the pocket structure is very
different to Carabodidae
(see Fernandez et al. 2013a)
. 2) The complexity of the locking
structure in Nippobodidae, specifically the longitudinal depression where tibia and
tarsus IV are inserted, femur IV which functions as a lid, and the bean-shaped structure
where the claw rests, are dissimilar to what is observed in Carabodidae.
This work is based on research supported in part by the National Research Foundation
of South Africa (UID) 85288. Any opinion, findings, and conclusions or
recommendations expressed in the manuscript are those of the authors and therefore the NRF
does not accept any liability in regard thereto.
Alberti G , Fernandez N ( 1990a ) Aspects concerning the structure and function of the lenticulus and clear spot of certain oribatids (Acari: Oribatida) . Acarologia 31 : 65 - 72 .
Alberti G , Fernandez N ( 1990b ) Fine structure and function of the lenticulus and clear spot of Oribatids (Acari: Oribatida) . In: Andre HM , Lions J -Cl ( Eds) L'ontogènese et le concept de stase chez les arthropodes . Agar, Wavere, 343 - 354 .
Alberti G , Fernandez N , Coineau Y ( 2007 ) Fine structure of spermiogenesis, spermatozoa and spermatophore of Saxidromus delamarei (Saxidromidae, Actinotrichida , Acari). Arthropod Structure Development 36 : 221 - 231 . https://doi.org/10.1016/j.asd. 2006 . 11 .002
Alberti G , Fernandez N , Kümmel G ( 1991 ) Spermatophores and spermatozoa of oribatid mites (Acari: Oribatida) . Part II. Functional and systematical considerations. Acarologia 32 : 435 - 449 .
Alberti G , Norton R , Adis J , Fernandez N , Franklin E , Kratzmann M , Moreno A , Ribeiro E , Weigmann G , Woas S ( 1997 ) Porose integumental organs of oribatid mites (Acari: Oribatida) . Zoologica 48 : 33 - 114 .
Aoki J ( 1959 ) Die Moosmilben (Oribatei) aus Südjapan . Bulletin of the Biogeographical Society of Japan 21 ( 1 ): 1 - 22 .
Aoki J ( 1961 ) Notes on the oribatid mites (I) . Bulletin of the Biogeographical Society of Japan 22 ( 6 ): 75 - 79 .
Aoki J (1965a) Oribatiden (Acarina) Thailands . I. Nature and life in Southeast Asia 4 : 129 - 193 .
Aoki J ( 1965b ) Oribatid mites (Acarina: Oribatei) from Himalaya with descriptions of several new species . Journal of the College of Arts and Sciences, Chiba University 4 ( 3 ): 289 - 302 .
Aoki J ( 1970 ) The oribatid mites of the Islands of Tsushima . Bulletin of the National Science Museum 13 ( 3 ): 395 - 442 .
Aoki J ( 1981 ) Discovery of the second species of the genus Nippobodes from Ohsumi Islands (Acari: Oribatei) . Bulletin of the Biogeographical Society of Japan 36 ( 4 ): 29 - 33 .
Aoki J ( 1984 ) New and unrecorded oribatid mites from Amami-Ohshima Island, Southwest Japan . Zoological Science 1 ( 1 ): 132 - 147 .
Aoki J ( 1989 ) A revision of the family Nippobodidae (Acari: Oribatida) . Acta Arachnologica 38 ( 1 ): 15 - 20 . https://doi.org/10.2476/asjaa.38.15
Aoki J ( 2000 ) Two new species of the family Nippobodidae (Acari: Oribatida) from Yunnan, Southwest China, with a key to the species . In: Aoki J , Yin WY , Imadaté G ( Eds) Taxonomical Studies on the Soil Fauna of Yunnan Province in Southwest China . Tokai Univeristy Press, Tokyo, 1- 6 .
Two new species of the family Nippobodidae (Acari, Oribatida), including a description ... 139
Chen J , Wang H ( 2007 ) Taxonomic study on the family Nippobodidae (Acari: Oribatida) from China . Zootaxa 1464 : 45 - 63 .
Choi S ( 1996 ) Study of soil microarthropods Mt.Hanla in Cheju-do 1. Four new species of oribatid mites at Sangumburi . Korean Journal Applied Entomology 35 ( 4 ): 280 - 286 .
Fernandez NA , Alberti G , Kümmel G ( 1991 ) Spermatophores and spermatozoa of some Oribatid mites (Acari: Oribatida) Part I. Fine structure and histochemistry . Acarologia 32 : 261 - 286 .
Fernandez N , Theron P , Rollard C ( 2013a ) The family Carabodidae (Acari: Oribatida) I. Description of a new genus, Bovicarabodes with three new species, and the redescription of Hardybodes mirabilis Balogh , 1970 . International Journal of Acarology 39 ( 1 ): 26 - 57 . http://dx.doi.org/10.1080/01647954. 2012 .741144
Fernandez N , Theron P , Rollard C ( 2013b) Revision of the family Carabodidae (Acari: Oribatida) IV. Aftibodes anjavidilavai n .gen., n.sp., Rugocepheus joffrevillei sp . n, and redescription of the genus Rugocepheus Mahunka , 2009 . International Journal of Acarology 39 ( 6 ): 462 - 480 . https://doi.org/10.1080/01647954. 2013 .822928
Fernandez N , Theron P , Rollard C ( 2013c ) The family Carabodidae (Acari: Oribatida) V. The genus Congocepheus (second part), with a redescription of Congocepheus involutus Mahunka 1997, and descriptions of Congocepheus gabonensis and Congocepheus extactastesi sp . nov. Zoosystema 35 ( 4 ): 551 - 579 . https://doi.org/10.5252/z2013n4a8
Fernandez N , Theron P , Leiva S ( 2016 ) Revision of the family Carabodidae (Acari: Oribatida) XI. Congocepheus kardiae sp. nov. and Zimbabweae pluosiae gen . nov., sp. nov. from the Republic of Zimbabwe . International Journal of Acarology 42 ( 7 ): 341 - 357 . http://dx.doi. org/10.1080/01647954. 2016 .1199138
Grandjean F ( 1949 ) Formules anales, gastronomiques, génitales, aggénitales du développement numérique des poils chez les Oribates . Bulletin Société Zoologique France 74 : 201 - 225 .
Krantz G , Walter D ( 2009 ) A manual of acarology. Third edition . Texas Tech University Press, Lubbock, Texas, 807 pp.
Norton R , Behan-Pelletier V ( 2009 ) Suborder Oribatida . In: Krantz GW , Walter DE (Eds) A manual of acarology. Third edition . Texas Tech University Press, Lubbock, Texas, 430 - 564 .
Jeleva M , Vũ M ( 1987 ) New Oribatids (Oribatei, Acari), from the Northern Part of Vietnam . Acta Zoologica Bulgarica 33 : 10 - 18 .
Travé J , Vachon M ( 1975 ) François Grandjean 1882-1975 (Notice biographique et bibliographique) . Acarologia 17 ( 1 ): 1 - 19 .