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ZOOTAXA
ISSN 1175-5326 (print edition)
ISSN
1175-5334
(online edition)
Copyright © 2017 Magnolia Press
Zootaxa 4319 (1): 077
–
090
http://www.mapress.com/j/zt/
Article
77
https://doi.org/10.11646/zootaxa.4319.1.4
http://zoobank.org/urn:lsid:zoobank.org:pub:71D6F6A1-1BC0-44DC-9DD9-713A9889DECF
Disparrhopalites naasaveqw n. sp. from caves at Wupatki National Monument,
Arizona, synonymy of Dietersminthurus Palacios-Vargas, Cuéllar & Vázquez,
1998 with Disparrhopalites Stach, 1956 and composition of Songhaicinae
(Collembola: Sminthuridae)
ERNEST C. BERNARD
1
& J. JUDSON WYNNE
2
1
The University of Tennessee, Entomology & Plant Pathology, 2505 E.J. Chapman Drive, 370 Plant Biotechnology, Knoxville, TN
37996-4560, USA. E-mail: ebernard@utk.edu
2
Department of Biological Sciences, Merriam-Powell Center for Environmental Research, Northern Arizona University, Box 5640,
Flagstaff, AZ 86011, USA
Abstract
Disparrhopalites naasaveqw n. sp. is described from a cave at Wupatki National Monument, Arizona. It differs from D.
patrizii (Cassagnau & Delamare Deboutteville, 1953) in having pigment and a well-developed ungual cavity, and from D.
tergestinus Fanciulli, Colla & Dallai, 2005 by having pigment, 8+8 eyes and a well-developed ungual tunica. Dietersmint-
hurus enkerlinius Palacios-Vargas, Cuéllar & Vázquez, 1998 is transferred to Disparrhopalites Stach, 1956 as D. enker-
linius (Palacios-Vargas, Cuéllar & Vázquez, 1998) n. comb. The sminthurid subfamily Songhaicinae Sánchez-García &
Engel, 2016 (type genus Songhaica Lasebikan, Betsch & Dallai, 1980) is redefined and the genera Disparrhopalites,
Gisinurus Dallai, 1970, Soqotrasminthurus Bretfeld, 2005 and Varelasminthurus Da Silva, Palacios-Vargas & Bellini,
2015 are transferred to this subfamily. A key is provided for separation of included genera. Effects of climate change on
presumed cases of cave restriction in the American Southwest are discussed.
Key words: cave-restricted, climate change, key, taxonomy
Introduction
Sminthuridae s. str. is a diverse and common family of 33 genera and 257 species (Bellinger et al. 1996‒2017).
Members of this family are abundant primarily in mesic conditions, with the vast majority of species occurring in
surface habitats (Bretfeld 1999). Within Sminthuridae is a small group of six genera characterized by minute size,
reduced number of setae (6) in the apical whorl of the tibiotarsi and characteristic ungues with a spine-like tunica
and/or cavity-like region. Only 12 species have been described in these six genera (Table 1). The separation of
these genera is based on the presence/absence of neosminthuroid setae, presence/absence of a cavity in the unguis,
presence/absence of pretarsal setae, number of anterior setae on the dens and denticulation of the mucronal edges.
A new species of this group from a cave in the southwestern U.S. contains a selection of these characters and
necessitates a review of the status of these genera.
The objectives of this paper are to describe Disparrhopalites naasaveqw n. sp.; synonymise Dietersminthurus
Palacios-Vargas, Cuéllar & Vázquez, 1998 with Disparrhopalites Stach, 1956; transfer several sminthurid genera
to Songhaicinae Sánchez-García & Engel, 2016; and provide a key to this distinctive group of small-sized
Sminthuridae.
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Table 1. Species of Sminthuridae considered in this paper.1
1Galeriella liciniana Curcic, Lucic, Tomic, Makarov & Karaman, 2007 (Herzegovina) may be a member of this group and appears to resemble
D. tergestinus, but not enough detail is provided in the description for an informed decision.
2Formerly Dietersminthurus enkerlinius Palacios-Vargas, Cuéllar & Vázquez, 1998.
Species
Type locality
Habitat
Other taxonomic literature
Disparrhopalites enkerlinius (Palacios-Vargas,
Cuéllar &Vázquez, 1998) n. comb.2
Quintana Roo, Mexico
Epigeic
Disparrhopalites patrizii (Cassagnau & Delamare
Deboutteville, 1953)
Toulouse, France
Troglophile
Stach (1956), Delamare Deboutteville
& Bassot (1957), Dallai (1970, 1971),
Bretfeld (1999), Fanciulli et al. (2005)
Disparrhopalites tergestinus Fanciulli, Colla &
Dallai, 2005
Basovizza, Trieste, Italy
Troglobite
Disparrhopalites naasaveqw n. sp.
Wupatki National Monument, Arizona,
USA
Obligate
troglophile
Gisinurus maletestai Dallai, 1970
Apuan Alps, Tuscany, Italy
Epigeic
Nayrolles (1993), Bretfeld (1999)
Gisinurus orenensis Bretfeld, Poliakov & Broza,
2000
Mt. Carmel, Israel
Epigeic
Songhaica adoracionae Palacios-Vargas, Cuéllar
& Vázquez, 1998
Quintana Roo, Mexico
Epigeic
Songhaica nigeriana Lasebikan, Betsch & Dallai,
1980
Ile-Ife, Nigeria
Epigeic
Bretfeld (2005)
Songhaica soqotrana Bretfeld, 2005
Socotra Island, Yemen
Epigeic
Songhaica stylifer (Murphy, 1960)
Kenneba and Jatabaa, Gambia
Epigeic
Lasebikan et al. (1980)
Soqotrasminthurus hadiboensis Bretfeld, 2005
Socotra Island, Yemen
Epigeic
Soqotrasminthurus vanharteni Bretfeld, 2005
Socotra Island, Yemen
Epigeic
Varelasminthurus potiguarus Da Silva, Palacios-
Vargas & Bellini, 2015
Rio Grande do Norte State, Brazil
Troglophile
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Material and methods
Study area. Wupatki National Monument (WUPA), part of the Colorado Plateau Shrublands Ecoregion (Ricketts
et al. 1999), is located in north-central Arizona near the southern margin of the Colorado Plateau. It has an area of
143 km
2
with an elevational range of 1310 m along the Little Colorado River on the eastern boundary to 1705 m
near the southwestern corner of the monument. Vegetation consists of juniper savanna (Juniperus spp.), Colorado
Plateau arid grassland, and a variety of Colorado Plateau shrubland associations (Ricketts et al. 1999).
Physiography is comprised of mesas, plains, canyons, bluffs, and badlands, and formed of Mesozoic sedimentary
surface layers and overlaid with Tertiary volcanic layers. Topography is sculpted by episodes of tectonic-scale
geologic deformation in the western United States over the last 65 million years, causing extensive crustal folding,
deep faulting, and uplift in north-central Arizona. Localised uplift is probably related to volcanism in the
surrounding San Francisco Volcanic Field. One geologic feature, the Black Point Monocline, continues to rise and
deform, creating an extensive network of visible fractures and minor offset faults in the surface sedimentary rock
formations. Some of these features have expanded laterally to form subterranean “earth crack” fissures or caves
(Huntoon 1965, Bridgemon 1975, CRF 1976). Our field sampling effort was limited to four of the six largest earth
crack caves within this monocline.
Field sampling. Between 29 August and 11 September 2013 and 24 August and 7 September 2014, the second
author led several teams of technicians to conduct systematic arthropod inventories of four earth-crack caves at
WUPA. During both years, sampling took place in late August once the summer monsoons were underway.
Monsoon starting dates were 5 July 2013 and 3 July 2014 (NOAA 2015). Arthropods were collected as
encountered (opportunistic collecting), as well as from baits deployed in the estimated deep zones of each cave and
leaf litter traps along the length of each cave. All arthropod sampling locations were plotted on the final cave maps
(see Wynne 2014, 2015). Opportunistic collecting of arthropods as encountered is a commonly applied approach
(e.g., Holsinger et al. 1976, Christiansen & Bullion 1978, Wynne & Pleytez 2005). This technique was applied as
the team was in transit between sampling outings for both bait sampling and leaf litter trapping. Bait sampling is
commonly applied for sampling cave-adapted arthropods (Howarth et al. 2007; Wynne et al. 2014). We used sweet
potato, chicken liver, Portobello mushroom and blue cheese (e.g., Howarth et al. 2007, Wynne et al. 2014). Two to
three stations of each bait type were deployed within each sampling location. Baits were deployed for four days and
removed once sampling was completed. We deployed leaf litter traps with a water delivery system in the entrance,
twilight and estimated deep zones of each cave (zonal descriptions provided below). The water delivery system
was used to keep the litter wet and facilitate decomposition (Humphreys 1991). Trap construction consisted of
plastic rectangular food-storage containers (34.5 × 25.4 × 6.4 cm) with six wooden pegs bolted to the lid of the
container and a screen stapled to the bottom of the pegs. The bottom of the container was used to contain both
leaves and arthropods once sampling was completed and traps removed. We used leaves of Gambel oak (Quercus
gambelii Nutt.) as leaf-litter “bait.” Leaves were heated with a lamp to reduce possible arthropod inhabitants but
were not sterilised.
Cave codes. At the request of WUPA staff, we used cave codes rather than actual cave names for all caves on
National Park Service lands. A copy of this paper, which includes a table of cave names with associated cave
codes, is on file with the Three Flagstaff Parks Headquarters, Flagstaff, Arizona and the National Cave and Karst
Research Institute, Carlsbad, New Mexico. Coordinates given in description represent general area where all caves
occur.
Preservation and observation. Specimens were cleared in heated Marc Andre I solution and either mounted
whole or dissected in Hoyer’s medium. Slides were dried in a 50°C oven for three days, then ringed with red
insulating varnish (MG Chemicals, Burlington, Ontario). Whole specimens were imaged with a Canon EOS T3i
camera mounted on a Zeiss Stemi 2000 stereo microscope. Body details were imaged with a 14-megapixel Q-
Camera on an Olympus BX-63 DIC microscope system or with a 17-megapixel DP73 camera on an Olympus BX-
53 phase contrast microscope. Measurements were made with the measuring software on the two microscope
systems. Full body images are provided in corrected colour; colours of detail images were adjusted for clarity of
structures and may not represent the actual colour of the feature presented. Most high-magnification images were
contrast-enhanced with software in the Olympus system.
Terminology. Names of setae and setal groups are adapted from Baquero et al. (2003) for head setae and
Betsch & Bretfeld (1991) for some aspects of thoracic and abdominal setae. The formula for anterior dental setae
follows Betsch (1980). Abbreviations used in this paper are as follows: Ant. I, Ant. II, Ant. III, Ant. IV for antennal
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segments; Th. II, Th. III for the mesothorax and metathorax; Abd. I, Abd. V, Abd. VI for the first, fifth and sixth
abdominal segments. Papillae and guard setae of the labial palpus are labelled according to Fjellberg (1999).
Caves are zonal environments often consisting of four principal zones: (1) an entrance (or light) zone
representing a combination of both surface and cave climatic conditions; (2) a twilight zone where light is
diminished and surface climate conditions are progressively dampened; (3) a transition zone characterized by
complete darkness with a further diminished influence of surface climate conditions; (4) a deep zone (usually the
deepest portion of the cave) where environmental conditions (e.g., complete darkness, temperature, and air flow)
remain relatively stable over time and the evaporation rate is negligible (Howarth 1980, 1982). We provide zone
designations for all Collembola specimens in the Material Examined section.
For springtail functional groups we use two commonly applied cave-specific terms, troglobites and
troglophiles (Barr 1968; Howarth 1983), and re-introduce a third term, obligate troglophiles (Peck 1970).
Troglobites are troglomorphic animals requiring cave deep zones, as well as human-inaccessible cracks and pore
spaces with similar habitat conditions, to complete their life cycle. Troglophiles are animals that occur facultatively
within caves (and human inaccessible cracks and pore spaces) and complete their life cycles there, but may also be
found in similar “cave-like” surface environments. Obligate troglophiles, first proposed by Peck (1970), are taxa
known to occur only in caves but lack troglomorphic characters.
Taxonomy
Family Sminthuridae Lubbock, 1862 sensu Betsch, 1980
Subfamily Songhaicinae
Songhaicinae Sánchez-García & Engel, 2016: 12.
Type genus. Songhaica Lasebikan, Betsch & Dallai, 1980
Updated diagnosis of Songhaicinae. Small species less than 1 mm long. Eyes present, rarely absent. Ant. IV
with 10‒26 subsegments. Tibiotarsus of all legs with six or fewer setae in apical whorl. Unguis usually with
prominent cavity and tunica, sometimes free apically as filament; if cavity absent, filament present. Unguiculus
typically truncated along inner edge, without or with very short terminal filament. Tenent hairs acuminate.
Neosminthuroid setae present or absent. Anterior surface of dens with 5‒13 setae. Mucro without subapical notch.
Subanal appendage tapering, smooth or with a few minute serrations near tip, pointing posteriorly.
Genera and species. See Table 1 for names and authorities.
Relationships within Songhaicinae. Recently, Songhaica was transferred to its own subfamily (Sánchez-
García & Engel 2016) with the following diagnostic characteristics: “three pairs of sminthuroid [= neosminthuroid]
setae, a few anterior setae on the dens, and the mucro lacking a subapical incision.” Only this last mucronal
character fits all of the species listed in this paper; neosminthuroid setae are present only in Songhaica and most
species have more than five anterior dental setae. Songhaica spp. have a cavity in the unguis (Bretfeld 2005), which
corresponds to the other 10 species of this group, except for D. tergestinus. However, the presence of a well-
developed tunica occurs in all species of the group except Songhaica spp. In addition, all those species that have
the apex of the tibiotarsus adequately illustrated have only six setae in the apical whorl. The combination of these
characters (six apical tibiotarsal setae, ungual cavity, well-developed tunica) serves as a rationale to unite the 13
species in the same subfamily. The significance of neosminthuroid setae as a subfamily characteristic is difficult to
estimate since the sminthurid subfamily Sphyrothecinae also possesses them (Bretfeld 1999), as does Sminthurinus
Borner, 1901 (Katiannidae) (Bretfeld 1999) and Neelidae (Richards 1968). Therefore, the presence of no more than
six setae in the apical tibiotarsal whorl and the combination of a filamentous tunica and/or ungual cavity serve
better to characterise this subfamily within Sminthuridae.
Relationships with other sminthurid subfamilies. Betsch (1980) proposed two subfamilies for Sminthuridae
(Sphyrothecinae and Sminthurinae), an arrangement followed by Bretfeld (1999). Songhaica was considered by
Bretfeld (1999) to be intermediate in position between Sphyrothecinae and Sminthurinae, but primarily allied with
Sminthurinae. Sánchez-García & Engel (2016) established Songhaicinae with a very brief diagnosis and without
direct comparison to the other subfamilies. Sphyrothecinae and Songhaicinae are similar in usually having fewer
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than 20 subsegments in Abd. IV. However, species of Sphyrothecinae possess neosminthuroid setae and modified
setae on the abdomen, lack a spine-like tunica and cavity on the unguis, and have tapering unguiculi with short or
long terminal filaments. All songhaicine taxa except Songhaica spp. lack neosminthuroid setae, which are
considered a diagnostic feature of Sphyrothecinae (Betsch 1980). Songhaicinae and Sminthurinae have
overlapping ranges for the number of anterior dental setae (5-13, 9‒15, respectively), but shapes of the unguis and
unguiculus are distinctly different.
All of the species included here in Songhaicinae that are sufficiently illustrated have six or fewer setae in the
apical whorl of the tibiotarsus. This character has not typically been included in sminthurid descriptions, but in
those where they are illustrated (e.g., Betsch 1980; Delamare Deboutteville & Massoud 1964; Nayrolles 1995;
Yosii 1959) tibiotarsi of Sminthurinae and Sphyrothecinae have more than six apical setae.
Disparrhopalites Stach, 1956
Disparrhopalites Stach, 1956:63.
Dietersminthurus Palacios-Vargas, Cuéllar & Vázquez, 1998:13, new synonym.
Type species: Disparrhopalites patrizii (Cassagnau & Delamare Deboutteville, 1953)
Other species:
D. enkerlinius (Palacios-Vargas, Cuellar & Vazquez, 1998) n. comb.
D. naasaveqw n. sp.
D. tergestinus Fanciulli, Colla & Dallai, 2005
Pararrhopalites patrizii Cassagnau & Delamare Deboutteville, 1953 was transferred to the new genus
Disparrhopalites by Stach (1956). This widespread European species (Dallai 1971, Fanciulli et al. 2005) has been
collected and studied thoroughly since then (Christian 1998; Dallai 1970, 1971; Delamare Deboutteville & Bassot
1957; Fanciulli et al. 2005; Gama 1988, 2005; Marx & Weber 2013, 2015). However, Disparrhopalites was not
compared to more recently described but clearly similar genera (Dietersminthurus, Gisinurus, Songhaica,
Soqotrasminthurus, Varelasminthurus, see Tables 1 & 2 for authorities and dates), perhaps because the two known
Disparrhopalites spp. lack a prominent cavity-like formation on the unguis. The type species, D. patrizii, possibly
a weak troglophile, has a shallow linear cavity while the highly modified troglobiont D. tergestinus apparently
lacks the cavity completely. Disparrhopalites naasaveqw n. sp., a presumed obligate troglophile, is very similar to
D. patrizii but has a distinct ungual cavity. The ungual cavity may be a synapomorphy for this small clade of
species that secondarily disappears with increasing troglomorphy. This scenario could account for the reduction of
the cavity in D. patrizii and its complete loss in D. tergestinus, as well as its retention in D. enkerlinius and D.
naasaveqw n. sp.
The monospecific genus Dietersminthurus was differentiated from similar genera by the presence of 5+5 eyes
and eight setae on the anterior face of the dens (Palacios-Vargas et al. 1998). The reduction in eye number is
recognised in a few other sminthurid genera, and the number of dental setae can be species-specific in several
genera, e.g., Sminthurus s. str. Latreille, 1802 (see Bretfeld 1999) and Sminthurinus Börner, 1901 (Christiansen &
Bellinger 1998). Ungual structure in D. enkerlinius appears to be identical to that of D. patrizii except that the
ungual cavity is well-developed in D. enkerlinius and weakly developed in D. patrizii, and D. enkerlinius possesses
eight anterior dental setae while D. patrizii has nine. Disparrhopalites naasaveqw n. sp. bridges these species by
having a patrizii-like unguis with a well-developed enkerlinius-like cavity and nine anterior dental setae as in other
Disparrhopalites spp. Therefore, Dietersminthurus is considered a junior subjective synonym of Disparrhopalites,
and its sole species, Dietersminthurus enkerlinius, becomes Disparrhopalites enkerlinius (Palacios-Vargas, Cuéllar
& Vázquez, 1998) n. comb.
Varelasminthurus was separated from similar genera by the absence of the posterior pretarsal seta (Da Silva et
al. 2015). The number of pretarsal setae of Disparrhopalites naasaveqw n. sp. varies (1 or 2) from leg to leg, and
therefore this character may not have significant validity at the generic level in Songhaicinae. However, the tunica
of the single species, V. potiguarus Da Silva, Palacios-Vargas & Bellini, 2015, is heavy and fused to an external
crest-like, serrated pseudonychium (Da Silva et al. 2015). Therefore, despite its similarities with Disparrhopalites
spp. it is maintained here as a valid genus.
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Disparrhopalites naasaveqw n. sp.
Figs. 1‒22
Material Examined. Holotype male dissected and mounted on 4 slides, paratype female on slide and three
paratypes in ethanol, USA, Arizona, Coconino County, Wupatki National Monument, UTM 457484, 3937066,
Zone 12S, cave WUPA-004, entrance/light zone, leaf litter trap #1, 09 September 2013. Same locality, cave
WUPA-001, 11 September 2013, one paratype male and one paratype female on slides, one paratype in ethanol,
entrance/light zone, leaf litter trap #1; one paratype male on slide, one paratype in alcohol, cave WUPA-001,
transition zone, leaf litter trap #6. All specimens collected by J.J. Wynne.
The holotype (WUPA 29654) and paratypes (WUPA29655‒29661) are deposited at the Museum of Northern
Arizona in the Wupatki National Monument Collection, Flagstaff, Arizona.
FIGURES 1‒7. Disparrhopalites naasaveqw n. sp. 1, 2) Dorsal and lateral views. 3) Basal knob and oval organ on hind
trochanter. 4) Distal setula of hind femur. 5) Pretarsal region of foreleg, pretarsal seta present on only one side (arrow). 6)
Pretarsal region of hind leg, pretarsal setae on each side (arrows). 7) Subanal appendage. Scales: Figs. 1, 2: 500 μm; Figs. 3, 5,
6: 10 μm; Fig. 4: 5 μm; Fig. 7: 20 μm.
Description. Males and females similar in length and appearance. Length 0.69‒0.86 mm (n = 5). Distinct
segmental sutures not seen on thorax and large abdomen; Abd. V fused with large abdomen. In ethanol,
pigmentation mottled, reddish violet to grey-violet (Figs. 1, 2), extent and intensity variable. Head pigmentation
varying from region between eye patches to covering most of frontal and genal regions. On large abdomen pigment
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generally covering anterior half and most of lateral region, and forming mid-dorsal band resulting in two large,
white, angular dorsal spots; pigment sometimes confined mostly to lateral region, dorsal white spots weakly
formed. Small abdomen pigmented antero-dorsally, pale elsewhere. Antennae and legs pale violet, venter and
furcula pale. Secondary granulation of large abdomen limited largely to dorsal and lateral setose regions; ventro-
lateral and ventral regions with primary granulation only (Fig. 18). Eight ocelli of similar size in each eyepatch
(Fig. 8).
Ratios of Ant. I‒IV 1: 1.7: 3.6: 10.4 . Ant. IV with 14‒15 subsegments. Terminal subsegment partially divided,
twice length of penultimate subsegment, with spherical apical bulb, thin apical sensillum-like seta; sensilla
arranged as one short and two long distal sensilla and three proximal sensilla (Figs. 10, 11). Penultimate
subsegment with three sensilla and seven typical setae in a single whorl, more proximal subsegments with two
sensilla and eight typical setae. Ant. III sense organ with two sense clubs in common pit and lateral conical
sensillum (Fig. 12).
Labial palpus (Fig. 9) with papillae A‒E present, bases weakly annulated; guard seta a1 displaced, long,
curved, extending laterally past palpus edge; b1 and b2 prominent, long, base of b1 expanded; b3 and b4, stout,
conical, b4 on upper side of palpus, behind other b-guards; d1 and d2 guards longer than d3 and d4; three e-guards,
e2 the longest, e3 very short; lateral papilla slender, pointed. Maxillary palpus with seta and two sublobal hairs. Six
prelabral setae. Labrum with three longitudinal lobes thinner than rest of labrum. Labral setae in three rows, 5-5-4
setae proximal to distal (Fig. 8); outer setae of proximal row and middle setae of distal row longer than neighbors.
Legs similar, increasing slightly in length from fore to hind leg; all leg setae smooth. Fore, middle and hind coxae
with 1, 1, 4 setae, respectively. Fore and middle trochanters each with four setae and two oval organs, hind trochanter
with five setae, two oval organs and stout, tapering, hooked spine Fig. 13). All femora with very short seta near
midpoint and minute spine-like setula near apex (Figs. 4, 13). Fore-femur with 14 typical setae, without oval organ;
middle femur with 15 typical setae, oval organ in basal half; hind femur with 17 typical setae, with oval organ in basal
third (Fig. 13). Tibiotarsi long and slender, with 6 setae at distal end; tenent hairs absent. Middle tibiotarsus with oval
organ in basal fourth, oval organs absent on fore and hind tibiotarsi. Anterior pretarsal seta present, socket weak;
posterior pretarsal seta randomly minute or absent (Figs 5, 6). Foot structure (Fig. 14) similar on all legs. Tunica
prominent, extending to and forming rounded tip of unguis, and with free filament originating at middle of unguis;
pseudonychium present, smooth or with minute denticles just at the limit of light optics; interior ungual edge with 8 or
9 teeth along most of its length. Unguis with internal, oval cavity. Unguiculus parallel-sided proximally, truncated
distally on interior side, with about 6 small teeth on it, and with conical cavity; external edge smooth.
Ventral tube with 1+1 lateral setae on corpus and 1 posterior seta on each valve; each membranous vesicle
with row of tubercles running its length and short row of tubercles distally (Fig. 15). Tenaculum with 2+2 teeth and
basal appendage, corpus with 2 or 3 setae; third seta, if present, medial (Fig. 16). Ratio of manubrium:dens:mucro
approximately 1:2.6:1.1. Manubrium with 8+8 posterior setae, without anterior setae. Dens smooth, with 25 lateral
and posterior setae; anterior setae arranged as 3,2,2,1…1 (Fig. 17). Both edges of mucro with small serrations.
Male genital plate (Fig. 22) with 12 to 13 setae: 2+2 lateral setae on margin, 8+8 or 7+8 small typical setae in the
middle of each side and 3+3 stouter, less dense setae interiorly, the most posterior of these thicker than the others.
Female genital plate not clearly seen. Subanal appendage of female (Fig. 7) tapering, pointed, curved distally, with
minute serrations near tip, pointing posteriorly.
Chaetotaxy. All typical head and body setae appearing smooth, of similar length. Setae of head and body usually
displaying minor asymmetry. Clypeal region with seven rows of setae posterior to prelabral row (Fig. 8): anterior
clypeal (ca), anterior clypeal-medial (cma), clypeal-medial (cm), anterior clypeal-central 1 (ccb), posterior clypeal-
central 2 (cca), clypeal-posterior (cp) and genal (g); 1+1 setae between cm and ccb rows; one oval organ near most
medial g-seta. Medial setal pair of one or more rows occasionally replaced by single mid-dorsal seta. Interantennal-
ocular area with d and sd-seta rows; d1 and d5 as single mid-dorsal setae; sd-setal row distinctly zig-zag.
Mesothorax without setae, metathorax with 4+4 setae, Abd. I with single row of 5+5 setae. Bothriotricha A‒C
nearly in straight line, B slightly anterior to line A-C, closer to C than to A (Fig. 18). Bothriotrix D very long,
slender, flexuous, arising from low multi-lobed tubercle with five accessory setae (Fig. 19). Chaetotaxy of small
abdomen similar in both sexes, with three middorsal setae (Figs. 20, 21). Males with two oval organs, females with
one oval organ on each side of Abd. VI. Neosminthuroid setae absent.
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FIGURES 8‒22. Disparrhopalites naasaveqw n. sp. 8) Head, anterior view. 9) Labial palpus. 10) Apex of Ant. IV, dorsal view.
11) Apex of Ant. IV, ventral view. 12) Apex of Ant. III. 13) Hind leg, coxa-trochanter-femur and tibiotarsus. 14) Hind foot. 15)
Ventral tube, posterior view. 16) Tenaculum. 17) Furcula, with manubrium and left dens in posterior view, right dens in anterior
view. 18) Chaetotaxy of thorax and abdomen, lateral view, male. 19) Bothriotrix D and associated setae. 20) Abd. VI, dorsal
view, male. 21) Abd. VI, lateral view, male. 22) Male genital plate. Abbreviations: ca = clypeal anterior, cma = clypeal medial
anterior, cm = clypeal medial, cc = clypeal central with rows a and b, cp = clypeal posterior, g = genal, ov = oval organ, ssl =
short seta, stl = setula (minute seta). Scales: Figs. 8, 15, 18: 100 μm; Figs. 9, 14: 10 μm; Figs. 10‒12, 16, 19, 22: 20 μm; Fig. 13:
25 μm; Figs. 17, 20, 21: 50 μm.
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TABLE 2. Differentiating characters for species listed in this paper, adapted from table in Da Silva et al. (2015).
1
1
Question mark indicates character is not described or illustrated in original or subsequent descriptions.
2
Text in Palacios-Vargas et al. (1998) states 5+5, illustration suggests 8+8.
3
Lasebikan et al. (1980) indicate 8+8 eyes for Gambian type specimens; Bretfeld (2005) states 6+6 eyes for Socotra specimens.
4
“Present” indicates that the species was illustrated with both pretarsal setae. A question mark indicates that this character cannot be determined
from the description or illustrations.
Genera and species Eye number Ant. IV
subsegments
Tenacular
setae
Posterior
pretarsal seta
4
Dens anterior setae Mucro
edges
Neosminthuroid
setae
Abd. V lobe,
bothriotrix D
Disparrhopalites enkerlinius n.
comb.
5+5 (8+8)
2
12 1+1 present 8 (3,2,2…1) serrate absent Short lobe, D
v
ery long, slender
Disparrhopalites
naasaveqw
n. sp.
8+8 14‒15 1+1 or 3 present or
absent
9 (3,2,2,1…1) serrate absent Short lobe, D
v
ery long, slender
Disparrhopalites patrizii 8+8 12 1+1 present 9 (3,2,2,1…1) serrate absent Short lobe, D
v
ery long, slender
Disparrhopalites tergestinus 0+0 14 1+1 ? 9 (3,2,2,1…1) serrate absent Short lobe, D
long, slender
Gisinurus maletestai 8+8 15 1+1 ? 13 (3,2,2,2,2,1…1) serrate absent Short lobe, D
long, slender
Gisinurus orenensis 8+8 13‒14 1+1 present 11 (3,2,2,2,1…1) serrate absent ?
Songhaica adoracionae 8+8 11 1+1 present 5 (3,1…1) smooth present Short lobe, D
long, slender
Songhaica nigeriana 8+8 (6+6)
3
10‒11 1+1 present 5 (3,1…1) smooth present Moderate lobe, D
slender
Songhaica soqotrana 6+6 11 1+1 present 5 (3,1…1) smooth present ǫ
Songhaica stylifer 6+6 10 1+1 ? 5 (3,1…1) smooth present ǫ
Soqotrasminthurus hadiboensis 8+8 20 2+2 ? 12 (3,2,2,2,1,1…1) smooth absent Long lobe; D
spine-like, short
Soqotrasminthurus vanharteni 8+8 26 2+2 ? 12 (3,2,2,2,1,1…1) smooth absent Short lobe; D
spine-like, short
Varelasminthurus potiguarus
8+8 11 1+1 absent 7 (3,2,1…1) smooth absent Short lobe, D
v
ery long, slender
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Etymology. The species name is the Hopi Native American term naasaveqw (naa-sah-vak) meaning “in the
middle”, referring to the mixture of characters that unite Disparrhopalites and Dietersminthurus. The Hopi are a
Puebloan People whose historical aboriginal boundary includes the present-day Wupatki National Monument.
Diagnosis. Disparrhopalites naasaveqw n. sp. is similar to D. patrizii in the nearly identical profile of the
claws, arrangement of anterior dental setae, and shape and dentation of the mucro. The two species differ in colour
(D. naasaveqw distinctly pigmented, D. patrizii white or slightly pigmented) and internal structure of the unguis
(distinct cavity in D. naasaveqw, no distinct cavity in D. patrizii). The new species and D. enkerlinius n. comb. are
similar in claw structure, antennal and mucronal features, and absence of Th. II setae (according to the illustration).
They differ in arrangement and number of anterior dental setae (see Table 2) and perhaps in the number of eyes. In
the original description of D. enkerlinius (Palacios-Vargas et al. 1998) the eye number is stated in two places as
5+5, but the head illustration seems to show 8+8. The other member of the genus, the troglobite D. tergestinus, is
blind, lacks pigment, has greatly elongated antenna and possesses long, thin ungues without teeth but with a
slender, free tunica.
Disparrhopalites naasaveqw n. sp. also bears some resemblance to Varelasminthurus potiguarus Da Silva,
Palacios-Vargas & Bellini, 2015 in presence of oval organs and sometimes having the posterior pretarsal seta
absent, but differs in anterior dental chaetotaxy (3,2,2,1…1 in D. naasaveqw n. sp., 3,2,1…1 in V. potiguarus),
development of tunica filament (long and thin in D. naasaveqw n. sp. vs. short and thick in V. potiguarus), and Th.
II setae (lacking in D. naasaveqw n. sp., 1+1 in V. potiguarus).
Disparrhopalites naasaveqw n. sp. is a presumed obligate troglophile lacking any characters suggestive of
troglomorphy.
Key to sminthurid genera with spine-like tunica and/or ungual cavity (Songhaicinae)
1. Neosminthuroid setae present; unguis without free tunica; anterior surface of dens with five setae . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Songhaica Lasebikan, Betsch & Dallai, 1980
- Neosminthuroid setae absent; unguis with or without spine-like tunica; anterior surface of dens with seven or more setae . . .2
2. Bothriotrix D short, stiff, spine-like; tenaculum with 2+2 setae. . . . . . . . . . . . . . . . . . . . . . . Soqotrasminthurus Bretfeld, 2005
- Bothriotrix D long, slender and flexible; tenaculum with 2 or 3 setae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .3
3. Tunica free apically as thin to thick spine; anterior face of dens with eight or more setae . . . . . . . . . . . . . . . . . . . . . . . . . . . . .4
- Tunica broad, appressed to ungual body; anterior surface of dens with seven setae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Varelasminthurus Da Silva, Palacios-Vargas & Bellini, 2015
4. Anterior surface of dens with 8 or 9 setae; free part of tunica thin, elongated, needle-like . . . . . . Disparrhopalites Stach, 1956
- Anterior surface of dens with 11‒13 setae; free part of tunica short, thick. . . . . . . . . . . . . . . . . . . . . . . . .Gisinurus Dallai, 1970
Discussion
Troglophiles and troglobites are infrequently encountered in Sminthuridae. Three species across three separate
genera are considered troglophiles (Caprainea marginata (Schött, 1893), Disparrhopalites patrizii and Lipothrix
lubbocki (Tullberg, 1872)) (Bretfeld 1999, Massoud & Thibaud 1973). Only two species (D. tergestinus and
Galeriella liciniana Curcic, Lucic, Tomic, Makarov & Karaman, 2007) are adapted as troglobites (Fanciulli et al.
2005, Curcic et al. 2007). The European cave species D. tergestinus is distinct from the other Disparrhopalites spp.
in its many adaptations to the cave environment. Based on a compilation of European records, Dallai (1970)
hypothesised that D. patrizii was a widespread species that evolved toward cave adaptation during the Quaternary
Period, a period of frequent widespread glaciation. Extending Dallai’s hypothesis, the large differences between D.
tergestinus and the other members of the genus could have been a consequence of differential selection, such as
genetic drift, or a far more ancient occupation of caves by D. tergestinus than in the other species (Fanciulli et al.
2005).
Species of Songhaicinae (Table 1) are generally epigeic, with only one troglobite and three somewhat dubious
troglophiles. Given there are numerous entrances and skylights associated with the Wupatki earth cracks, airflow
and moisture may move through these features in a similar manner to lava tube caves. Wynne and Shear (2016)
suggested that cooler temperatures and higher humidity in New Mexico lava tubes provided conditions appropriate
for a presumed cave-restricted relict species of millipede that occurred in the entrance of one cave. On the surface
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near where this millipede is known to occur, leaf-litter accumulation is limited in the lava beds with low conifer
tree cover and suitable habitat for this species is largely lacking; therefore, earth cracks may provide a similar sort
of refugium.
Disparrhopalites naasaveqw may represent yet another example of an obligate troglophile (i.e., an animal
restricted but not adapted to the cave environment). Historically, the “climatic relict hypothesis” has been used to
explain the occurrence and isolation of troglomorphic taxa found in the temperate regions of the world (Jeannel
1943; Barr 1968). Wynne and Shear (2016) proposed that a new species of millipede, Austrotyla awishoshola
Wynne & Shear, 2016 (from western New Mexico), lacking characteristics of cave adaptation, was restricted to
cave moss gardens, and perhaps also the crevices and mesocaverns within the lava beds of the region. This animal’s
restriction to the subterranean environment may have happened during the climatic oscillations at the end of the
Pleistocene. Similarly, we suggest D. naasaveqw is restricted to cave environment and may also be considered a
climatic relict. Given the habitat requirements of other Disparrhopalites species, this animal may have been quite
common on the surface when conditions were more mesic and leaf litter was present.
We acknowledge the inherent difficulties of definitively assigning functional groups to cavernicolous species.
Adequate sampling of both cave and surface ecosystems is essential to best assign functional groups for species
detected within caves (Trajano and Carvalho 2017). Furthermore, evolutionary plasticity in these functional groups
should be recognized, and detailed morphological, physiological and behavioral analyses are often required to
determine if a given species lacks troglomorphic (cave-adapted) adaptations. Mindful of this, Sket (2005) proposed
an expansion of troglobiont (first proposed by Racovitza 1907) by merging troglobite (= troglobiont) and obligate
troglophile into one category. Similarly, Trajano and Carvalho (2017) considered “troglobites” to represent two
types – troglomorphic and non-troglomorphic troglobites. We do not consider this proposal, either, to be a fruitful
approach. Combining presumed cave-restricted troglomorphic or non-troglomorphic animals into one category
may impede our ability to investigate evolutionary questions related to cave-restriction and accurately examine
community dynamics and niche selection of cavernicoles. Additionally, several non-troglomorphic cave-restricted,
climate-relict species are believed to be restricted to deep zones and small subterranean pore spaces (Shear et al.
2009). Non-troglomorphic arthropods restricted to relict habitats within cave entrances due to climatic shifts
(Benedict 1979, Wynne and Shear 2015) and extensive surface disturbance (Wynne et al. 2014, Bernard et al. 2015,
Taiti and Wynne 2015), have also been identified. These distinctions further underscore the need to resurrect
“obligate troglophile” for classifying non-troglomorphic, cave-restricted fauna.
Acknowledgements
We thank Paul Whitefield, National Park Service, who was instrumental in all aspects of permitting, logistics,
fieldwork planning and execution, and provided the study area description for WUPA. Leigh Kuwanwisiwma and
Terry Morgart, Hopi Cultural Preservation Office, provided us with the Hopi term to name the species. Gwenn
Gallenstein, curator for National Park Service museum collections at the Museum of Northern Arizona assigned
catalog numbers of specimens and provided long-term curation of holotypes and paratypes. Administrative support
was provided by Neil Cobb, Stefan Sommer and Marie Saul with the Merriam-Powell Center, Todd Chaudhry, NPS
Colorado Plateau, Cooperative Ecosystems Studies Unit (CESU), and Cindy Judge, NAU Grants and Contracts.
Greg Florian, NAU CEFNS Teaching and Research Machine Shop, mass-produced the leaf-litter traps. Joel
Dugdale, Scott Fray, Greg Flores, Kayla Lauger, Jeff Jahn, Patricia Kambesis, Isaac Shaffer and Reamy Winton
assisted with biological inventory and cave cartography fieldwork. Sergeant Aaron Dick and the Coconino County
Search and Rescue team, and NPS Law Enforcement remained on emergency stand-by during all field operations.
This project was funded through a Colorado Plateau-CESU cooperative agreement between Wupatki National
Monument and Northern Arizona University. The authors are grateful to the peer reviewers of this paper for their
insights and suggestions.
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