European Journal of Taxonomy 234: 1-17

http://dx.doi.org/10.5852/ejt.2016.234

This work is licensed under a Creative Commons Attribution 3.0 License.

ISSN 2118-9773

www. europeanj ournaloftaxonomy. eu

2016 • Miranda G.S. et al.

Research article

urn:lsid:zoobank.org:pub:7A78A076-8848-4FFF-A3C2-BlFA3A94DC2F

A new species of Charinus Simon, 1892 (Arachnida: Amblypygi:

Charinidae) from Israel and new records of C. ioanniticus (Kritscher, 1959)

Gustavo S. MIRANDA 1 *, Shlomi AHARON 2 , Efrat GAVISH-REGEV 3 ,

Alessandro P.L. GIUPPONI 4 & Gil WIZEN 56

1 Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark

(Zoological Museum), University of Copenhagen, Copenhagen, Denmark.

2 Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev,

Sede Boqer Campus, Midreshet Ben-Gurion, 849900, Israel.

3 The National Natural History Collections, The Hebrew University of Jerusalem,

Edmond J. Safra Campus, Jerusalem, 9190401, Israel.

4 Faboratorio de Referenda Nacional em Vetores das Riquetsioses,

FIRN-FIOCRUZ, Rio de Janeiro, RJ, Brazil.

5 Faculty of Forestry, University of Toronto, Toronto, Ontario M5S 3B3, Canada.

6 Department of Zoology, Tel Aviv University, Tel Aviv, 6997801, Israel.

* Corresponding author: smiranda. gustavo@gmail. com

2 Email: [email protected]

3 Email: [email protected]

4 Email: agiupponi@gmail com

5 Email: wizentrop@gmail com

1 urn:lsid:zoobank.org:author:AF7CC5D6-31CE-40D2-AClE-9D24245D19C4

2 um:lsid:zoobank.org:author:FB5EEA73-DD16-440C-B611-07FlC0C1300B

3 urn:lsid:zoobank.org:author:FC073F19-2202-4C89-8B43-CEA4CC5E2D50

4 urn:lsid:zoobank.org:author:434112AC-B212-43E8-A5D9-2F5D5619AFC4

5 urn:lsid:zoobank.org:author:08A8140A-AF25-4275-9A01-32BADF0DFB04

Abstract. A new species of Charinus is described from Israel and new localities for C. ioanniticus are

reported. Charinus israelensis sp. nov. is a cave dwelling species with extremely small median eyes,

no median tubercle and reduced lateral eyes. It is similar to C. ioanniticus , which occurs in nearby

areas, but can be differentiated by the shape of the carapace, the number of pedipalp spines and the

development of the eyes. A detailed comparison is made between the two species, including pictures,

drawings and scanning electron micrographs. Charinus ioanniticus is reported here from several new

localities in Israel and Turkey. Identification keys to the Charinus species groups and to the species of

the bengalensis group are provided.

Keywords. Biodiversity, caves, Palearctic, taxonomy, whip spider.

Miranda G.S., Aharon S., Gavish-RegevE., GiupponiA.P.L. &Wizen G. 2016. Anew species of Charinus Simon,

1892 (Arachnida: Amblypygi: Charinidae) from Israel and new records of C. ioanniticus (Kritscher, 1959).

European Journal of Taxonomy 234: 1-17. http://dx.doi.org/10.5852/ejt.2016.234

European Journal of Taxonomy 234 : 1-17 ( 2016 )

Introduction

Whip spiders are distributed in the tropical and sub-tropical regions of the world. Among the five

families, Charinidae Quintero, 1986 is the most diverse in the order, with 88 species, and the genus

Charinus Simon, 1892 is the largest of the family, with 70 described species. The majority of the known

species is found in the Neotropics (Giupponi & Miranda 2016; Miranda et al. 2016), and only three

charinids are known from the Indomalayan and Palearctic regions: Charinus bengalensis (Gravely,

1911), C. ioanniticus (Kritscher, 1959) and C. pakistanus Weygoldt, 2005. These species belong to the

bengalensis species group, which is characterized by the finger-like female gonopod. Two additional

species groups are recognized in this genus: the brasilianus and australianus groups, which have

sucker-lilce and cushion-like gonopods, respectively, and are found in the Americas, Africa and Oceania

(Weygoldt 2005).

Despite being a Pleistocene refugium for several taxa and having a high degree of endemism (Husemann

et al. 2014), the eastern Mediterranean counts thus far only one known species of Charinus , the

parthenogenetic C. ioanniticus. This species is recorded from Greece (Kritscher 1959), Turkey (Kovarik

& Vlasta 1996; Weygoldt 2005; Seyyar & Demir 2007), Egypt (El-Hennawy 2002) and Israel (Kraus

1961; Rosin & Shulov 1960). It is the most widespread species of the genus, probably as a consequence

of human activities, such as accidental transport with plants (Weygoldt 2005).

Whip spiders were found in a cave fauna survey in Israel (see Gavish-Regev et al. (2016) for details on

the cave survey), as well as from occasional collecting events in caves. Among the specimens collected,

several were noticeably different to the widespread species C. ioanniticus. We examined all whip spider

material found in Israel and present here new data on the distribution of C. ioanniticus in Israel and

Turkey. We also describe a new species, Charinus israelensis sp. nov. from a few different caves in

the northern region of Israel, and provide keys to the Charinus species groups and to the species of the

bengalensis group.

Materials and methods

Permits and repository collection

The specimens were collected with permits issued by the Nature and Parks Authority in Israel (permit

numbers 2012/38653, 2013/40027, 2014/40313 and 2014/40503). The animals were found through

visual searching along the walls and ceiling in the caves using a powerful LED headlamp. Specimens

were captured by hand and placed in vials containing 70% ethanol, and were later deposited in the Israel

National Arac hni d Collection of The Hebrew University of Jerusalem and the National Museum of Rio

de Janeiro. Some of the specimens were kept alive and taken to the laboratory for natural history and

behavioral observations. Live specimens were kept in 10x5^5 cm acrylic containers (AMAC Plastics

Ltd., California, USA) with moist peat substrate and a Styrofoam board placed diagonally as a resting

spot. They were kept at 24°-26°C in a dark room and were fed with live silverfish and cricket nymphs.

Laboratory procedures

The studied specimens were examined using a Leica M205C stereo microscope, which is attached to

a camera lucida used for the drawings. Photographs were taken with a BK+ Imaging System from

Visionary Digital t http://www. visionary digital, com ) equipped with a Canon EOS 7D camera at the

Zoological Museum, Copenhagen (Denmark). Single images were combined with Helicon Focus

(version 5.3; www.heliconsoft.com l software from Helicon Soft Ltd. to increase depth of field, and

further processed in Photoshop CC to adjust color, brightness and contrast, and remove blemishes. SEM

images were made with a JEOL JSM-6390 LV at Plataforma de Microscopia Eletronica Rudolf Barth,

FIOCRUZ-IOC, Rio de Janeiro (Brazil).

MIRANDA G.S. et al. , New species and records of Charinus

Measurements and nomenclature follow Quintero (1981) in general. The pedipalp article, called tarsus

by Quintero, is here divided into distitarsus and tarsal claw (pretarsus), as the two articles are not fused

in Charinidae. The measurements of pedipalp articles were taken between the external condiles of each

segment in order to establish fixed points and proper length measurements (Baptista & Giupponi 2002).

The sensilla names on the first leg follows Igelmund (1987). The measurements were taken from several

specimens (number indicated as “n-’) with the median value given first, followed by the range in

parentheses. The measurement accuracy is indicated in the legend of each figure.

The following abbreviations are used for museums and other collections:

AMNH

HUJINVAMB

MZUT

MHNG

MNRJ

NHMW

SMF

ZMUC

American Museum of Natural History, New York

National Arachnid Collection, The Hebrew University of Jerusalem, Jerusalem

Natural History Museum, Zoological Section ‘La Specola’ of the University of

Florence, Florence

Museum d’Histoire naturelle de Geneve, Geneva

National Museum, Rio de Janeiro

Naturhistorisches Museum Wien, Vienna

Senckenberg Museum, Frankfurt

Zoological Museum, Natural History Museum of Denmark, Copenhagen

Additional material analyzed

Charinus abbatei Delle Cave, 1986: holotvpe . Somalia, Grotta do Showli Berdi, Bardera, Tratto 20,

Campione 12, S.B.S.I., 15 Mar. 1984, Coll. 167 (1 $, MZUF 1896).

Charinus africanus Hansen, 1921: svntvpes . Sao Tome e Principe, Annobon, 400-500 m, May 1902,

L. Tea leg. (3 $$, ZMUC00024552); svntvpes . Sao Tome e Principe, St. Thome, Vista Alegre, 200-

300 m, Sep.-Oct. 1900, L. Tea leg. (2 specimens, ZMUC00024545). Non types: Sao Tome, near Sao

Nicolao waterfall, ca 800 m, 8-16 Oct. 2006, under stones and wood, leg. S.u.P. Weygoldt (2 $$, 2 $ 5,

1 juvenile, AMNH).

Charinus bengalensis (Gravely, 1911): holotvpe . India, West Bengal, Kolkata (as Calcutta), Indian

Museum (1 SMF 64590).

Charinus eleonorae Baptista & Giupponi, 2003: holotvpe . Brazil, Minas Gerais, Itacarambi, Grata Olhos

d’Agua, 26 Jun. 2001, R.L.C. Baptista and A.P.L. Giupponi leg. (1 MNRJ 9070); paratvpes . Brazil,

Minas Gerais: Itacarambi, Grata Olhos d’Agua, 26 Jun. 2001, R.L.C. Baptista and A.P.L. Giupponi leg.

(7 (?(?, 6 $ 5, 2 immature SS, 2 immature ?$, 2 juveniles, MNRJ 9033).

Charinus ioanniticus (Kritscher, 1959): svntvpes. Greece: Island of Rhodos, Lindos, below castle,

Paget, 3 Jul. 1969, Bilek leg. (1 5, NHMW 19138); Island of Rhodos, Lindos, Paget, 1963, Bilek leg. (5

55, NHMW 19137); same data (2 juveniles, NHMW 1427). Non-types . Greece: Rhodos, O. Bechtold

leg. (2 55> 3 juveniles, MHNG); Dodelcanes, Rhodos, Rhodos City, Jun. 1978, N. Polemikos leg. (1

5 , SMF 56704); Rhodos, Lindos, castle of Johannites [= Monolithos], in wall and rock fissures of the

substructure, 27 Apr. 1964, V. Helversen and H. Pieper leg. (6 55> SMF 17319; 4 55> SMF 17392);

Kos, bunker of the castle, 30 Apr. 1965, H. Piepper leg., O. Kraus det. (6 55» SMF 17391); Rhodos,

town of Lindos, Krichter leg. (1 5 , SMF 11895/1); Turkey: Iskenderan, Qevlik (Jeskyne), 36°07' N,

35°55' E, 3 Aug. 1998, Sobotnik leg. (2 MHNG); Adana, 12 km north of Kozan, under rock,

300 m, 5 May 1967, Cl. Besuchet leg., O. Kraus det. (1 MHNG); Yalan Dunya Cave, Beyrebucak

Village, Gazipa§a District, Antalya Province, Turkey, 36°13'16.92" N, 32°24'4.43" E, 5 Dec. 2013,

K.B. Kunt and Y.M.Marasik leg. (1 5 , ZMUC00042413). Israel: Carmel Ridge, Haifa, 32°47'47.50"

N, 35°0'59.47" E, 24 Jun. 2014, G. Wizen leg. (1 5 , HUJINVAMB 100); Haraba cave, 9 Mar. 2014,

European Journal of Taxonomy 234: 1-17 (2016)

Aharon and Gavish-Regev leg. (1 §, HUJINVAMB 119); Khirbet Roma, near Rumana, Beit Netofa

Lower Galilee, 32°47'20.39" N, 35°17'35.18" E, 178 m, 21 Mar. 2015, Ori Segev leg. (HUJINVAMB

120); Jerusalem, Rosin leg., 4 May 1960 (1 $, SMF 12126/1; 1 ?, SMF 12127/1).

Charinus pakistanus Weygoldt, 2005: holotype . Pakistan, Hazara, Malkandi, 1500 m, between Kawai

and Mahandri, sieving of dead leaves and old tree stumps in a deciduous forest, 3 Jun. 1983, Cl. Besuchet

and L Lobl leg. (1 $, MHNG); paratvpe . Pakistan, North-West Frontier Province, ca. 1.5 km N of

Islamabad, ca 800 m, forest under stones, 33°44'30" N, 73°03' E, 2003, S.V. Ovchinnikov leg. (2 SS,

3 ??, SMF 40168).

Charinus troglobius Baptista & Giupponi, 2002: holotvpe . Brazil: Bahia, Carinhanha, Serra do

Ramalho, Gruna do Ze Bastos, 28 Jun. 2001, R.L.C. Baptista and A.P.L. Giupponi leg. (1 <$, MNRJ

9067); paratvpes . Brazil, Bahia, Carinhanha, Serra do Ramalho, Gruna do Ze Bastos, 28 Jun. 2001,

R.L.C. Baptista and A.P.L. Giupponi leg. (9 2 $ §, MNRJ 9068); Gruna do Ze Bastos, 28 Jun. 2001,

R.L.C. Baptista and A.P.L. Giupponi leg. (1 §, MNRJ 9078).

Results

Arachnida Cuvier, 1812

Amblypygi Thorell, 1883

Family Charinidae Quintero, 1986

Genus Charinus Simon, 1891

Charinus israelensis sp. nov.

urn:lsid:zoobank.org:act:D789C530-EBA5-4774-817E-EBCA7DAC76EB

Figs 1-6

Diagnosis

Median eyes extremely reduced and median tubercle absent; lateral eyes very reduced; 6-8 frontal setae

on the carapace; basitibia of leg IV divided in four pseudo-articles; trichobothrium of the basitibia IV

(bt) at the proximal third of the article; distitibia IV with 16 trichobothria; trichobothrium be closer to

bf than to sbfi finger-like gonopods. It differs from C. ioanniticus, by the degree of development of the

median and lateral eyes, the number of spines on the pedipalp (femur with four dorsal and four ventral

in C. israelensis sp. nov. and five dorsal and five ventral in C. ioanniticus ), the shape of the carapace

(with a rounded frontal border in C. israelensis sp. nov. and projected anteriorly in C. ioanniticus ) and

the shape of the frontal process (acute in C. israelensis sp. nov. and rhomboid in C. ioanniticus ).

Etymology

The specific epithet, a Latin adjective, refers to the country where the new species was found.

Type material

Holotype

ISRAEL: §, Mimlach cave, Lower Galilee, 32°5E31.84" N, 35°26'34.94" E, Wizen G. leg., 30 Mar.

2014 (HUJINVAMB 111A).

Paratypes

ISRAEL: 1 §, locality and date as for holotype, Wizen G. leg. (HUJINVAMB 11 IB); 3 $ $, Susita cave,

Southern Golan Heights, 32°46'46.20" N, 35°39'28.53" E, 2 May 2013, Wizen G. leg. (2 in HUJINVAMB

109, 1 in MNRJ 9307); 1 §, same locality as holotype, 13 Jul. 2013, Wizen G. leg. (HUJINVAMB 110).

MIRANDA G.S. et al.. New species and records of Charinus

Fig. 1. Charinus israelensis sp. nov. A. Habitus, dorsal view. B. Sternum. C. Frontal view of pedipalp

distitarsus. D. Pedipalp, dorsal view. E. Pedipalp, ventral view. Scale bars: 1 mm.

European Journal of Taxonomy 23'4: 1-17 (2016)

Description

Female (n = 4)

Measurements (in mm). Carapace: length 3.0 (2.76-3.54), width 4.3 (3.92^1.86). Body total length:

8.1 (6.6-10.5). Pedipalp: Femur 2.7 (2.1-3.6), Tibia 3.0 (2.5—4.0), Basitarsus 1.3 (1.2-1.6), Distitarsus

0.9 (0.8-1.0), Tarsal claw 0.7 (0.6-0.9). Leg I: Femur 7.5 (6.9-9), Tibia 12.8 (11.5—15.3), Tarsus 13.4

(13.2-13.8). Leg II: Femur 5.0 (4.5-5.9), Basitibia 3.7 (3.4^1.4), Distitibia 2.5 (2.3-2.7), Basitarsus

1.0 (0.8-1.2), Other tarsal articles 0.7 (0.7-0.7). Leg III: Femur 5.8 (5.3-6.7), Basitibia 4.6 (4.2-5.4),

Distitibia 2.7 (2.5-3.0), Basitarsus 1.1 (1.0-1.3), Other tarsal articles 0.8 (0.7-0.9). Leg IV: Femur 4.9

(4.5M.8), Basitibia I 2.3 (2.1-2.8), Basitibia II 0.6 (0.5-0.8), Basitibia III 0.7 (0.6-0.9), Basitibia IV

1.2 (1.1-1.4), Distitibia 2.5 (2.2-2.8), Basitarsus 1.1 (0.9-1.3), Other tarsal articles 0.7 (0.6-0.9). Size

range is shown in Fig. 5A.

Carapace (Figs 1A, 4A). Carapace flattened, wider than long (1.4 times), strongly bent downwards

below lateral eyes; a thin median furrow reaches the fovea starting from the depression where remnants

of median eyes are present. Anterior margin rounded, with six to eight large frontal setae. Many tiny

Fig. 2. Charinus israelensis sp. nov. A. Last segment of basitibia and distitibia IV. B. Mesal view of

chelicerae, detail of the internal row of teeth in the basal segment. Abbreviations: be = basocaudal; bf=

basofrontal; bt = basotibial; sbf = sub-basofrontal. Scale bars: 1 mm.

MIRANDA G.S. et al.. New species and records of Charinus

Fig. 3. Charinus israelensis sp. nov., gonopod and leg I. A. Dorsal view of female gonopods. B. Detail

of the tip of the finger-like gonopod. C. Dorsal view of the first segments of tarsus I. D. Detail of the

tip of the first segment of tarsus I. Abbreviations: b = bristle; cl = club sensillum; me = modified claw.

European Journal of Taxonomy 234: 1-17 (2016)

Fig. 4. Carapace, frontal process and habitus. A, C-D. Charinus israelensis sp. nov. B, E-F. C. ioanniticus

(Kritscher, 1959). Scale bars: A-B =1.0 mm; C-E = 0.1 mm

MIRANDA G.S. et al ., New species and records of Charinus

punctuations, more abundant in frontal area; frontal process large, triangular, acute, not visible from

above. Three pairs of lateral furrows on carapace, and an oval fovea. 1st pair of furrows placed just behind

lateral protrusion; all furrows reach middle line. Eyes small, lateral eyes poorly or non-pigmented, but

with tapetum; median eye tubercle absent and eyes almost absent, only a pair of small dots with remnant

of lenses.

Sternum (Fig. IB). Tetra-segmented, all segments well sclerotized. Tritostemum with a round basis

and projected anteriorly in a small blunt tubercle, which roughly surpasses the base of the pedipalp

coxae, and with two apical, two median and two basal setae, and smaller ones at the base. Middle

segment rounded, convex, with two setae and a few small ones. Third segment also rounded and convex,

subequal to the middle segment, with two setae and several small ones. Sternites separated from each

Fig. 5. Live specimens of Charinus israelensis sp. nov. A. Two specimens showing the size range. B. $

carrying eggsacs, lateral view. C. $ carrying egg sacs, ventral view.

European Journal of Taxonomy 234: 1-17 (2016)

other by half the diameter of the middle segment. Metasternum simple, with two pairs of small setae in

a row on distal region.

) u

N T A

1 N S

O c • " ° K

Karam an

Turkey

v ^ Adana

r ' bin .Ony e

J- -"6 i

Mersin a T

i orsu ^

Alany a

O Ft O

Iskenderun

Antakya \

' O .

f •

Syria

0 20

40 80

Al Lad hi «|i yah

Cyprus

Fig. 6. Distributional map of Charinus Simon, 1892 in Turkey and Israel.

MIRANDA G.S. et al ., New species and records of Charinus

Abdomen (Figs 1A, 5B-C). Oblong, with almost indistinguishable punctuations, finer than those on the

carapace. Ventral sacs developed, without ventral sac covers. When carrying the eggsac, the abdomen is

slender and concave; the egg sac is wider than the abdomen, and no fold surrounds it.

Chelicera (Fig. 2B). Cheliceral furrow with four internal teeth; first tooth (upper) bifid, la slightly

smaller than lb. Second tooth geminated with the first (la + lb). Second and third teeth subequal. Fourth

tooth one third larger than II and III and subequal to lb. Teeth length: IV = lb > la > II = III. External row

with one small denticle in the upper region and small projection in the lower region. Internal surface of

basal article with a vertical row of 3-4 large setae. Claw with eight small denticles.

Pedipalp. Trochanter (Fig. IE): large ventral apophysis, located at posterior border of trochanter,

spiniform, bearing 13 large setae, with blunt tip pointed forwards; two subequal spines, one in about the

center of the anterior row of tubercles, the other at its distal end. Femur (Fig. 1D-E): four dorsal spines

(I > II > III > IV) with two prominent setiferous tubercles before first spine; four ventral spines with two

setiferous tubercles before the first spine (I > II > III > IV). Tibia (Fig. 1D-E): five spines (I > II > III >

IV > V); two setiferous tubercles distal to spine I, the proximal one about one third length of spine I and

the distal one a bit higher than a regular setiferous tubercle; spine II two thirds of spine I, and spine III

one third of spine I. Spines I and II with four setiferous tubercles on its first third. Three ventral spines

(I > II > III), the proximal one a bit larger than a setiferous tubercle. Basitarsus (Fig. 1D-E): two dorsal

spines, the basal one two thirds the size of the distal one. One ventral spine at distal half, two thirds the

size of basal dorsal spine. Distitarsus (Fig. 1C-E): two large curved spines, the distal half the size of

the article, and the basal half the size of the distal spine. Cleaning organ about half of the article length.

Claw (Fig. 1C): long, with an acute, curved tip.

Legs. All setose. Ventral corner of the prolateral face of femora II-IV projecting in a distinct spiniform

process. Femur length: I > III > II > IV. Tibia I with 21 articles. Tarsus (basitarsus + distitarsus) I with 37

articles; modified claw at tip of leg (Fig. 3C-D); leg covered with many bristles (b) and club sensilla (cl).

Leg IV: Basitibia: divided into four pseudo-articles, with one trichobothrium (Fig. 2A) on the proximal

third of the last pseudo-segments. Distitibia (Fig. 2A): two basal and 14 distal trichobothria (total of 16);

trichobothrium be closer to bf than to sbf which is displaced to close to sf-sc. Basitibia-distitibia length:

DT > BT1 > BT4 > BT3 > BT2.

Color pattern (in alcohol) (Figs 1, 4A). Chelicerae, pedipalps and carapace yellowish-brown. Legs

lighter colored. Abdomen pale yellow. Color of live animals (Figs 4D, F, 5): Chelicerae burgundy,

pedipalps and carapace reddish-brown. Some individuals have tiny spots of dark pigment anteriorly to

the depression that marks the location of the missing median eyes. Legs yellowish-brown. Abdomen

pale yellow. Egg sac tanned and dark brown. All setae red.

Genitalia. Female gonopod (Fig. 2A-B): posterior margin of genital operculum straight, with few setae

along its margin and on its surface. Gonopods finger-like appendage vestiges, forming a wrinkled and

folded cushion, with a broad base narrowing to a thin straight apical appendage vestige; deep in the

genital atrium. Gonopod very similar to that of its closest related species C. ioanniticus.

Male

Unknown.

Natural history

Charinus israelensis sp. nov. was found only in warm, humid man-made caves in northern Israel.

Females were collected from March to July (the caves were not visited in the autumn and winter season

to avoid disturbing a population of Rhinolophus bats that hibernate in the cave). Although we found

European Journal of Taxonomy 234: 1-17 (2016)

several small-sized arthropods in the caves (e.g., Blattodea, Thysanura), the most frequently encountered

prey items were spiders of the genus Loxosceles and isopods. Juveniles of C. israelensis sp. nov. feed

mainly on Psocoptera dwelling on the cave floor. This species is tolerant to conspecifics compared to

other Charinus species, with individuals often found in close proximity (ca 20 cm) to each other. Gravid

females are more isolated and show aggression towards other individuals (Fig. 5A). The egg sac contains

9-30 eggs (Fig. 5B-C). Egg measurements: 1.3-1.4 mm in diameter. At 25°C, egg development takes

ca 90 days. The hatching praenymphae are white and measure 2-2.2 mm. They climb and stay on the

mother’s back for 12 days, after which they molt into protonymphae measuring 2.5 mm in length.

Distribution

Known from the type locality (Mimlach cave, Lower Galilee) and from Susita, Southern Golan Heights,

both in northern Israel (Fig. 6).

Key to the Charinus species group and to the species of the bengalensis species group

The three Charinus species groups ( australianus , bengalensis and brasilianus) can be identified by the

different shape of the female genitalia (Weygoldt 2005). Here we provide a key to the species groups of

Charinus , including references to images of each type of female gonopod, and a key to aft species of the

bengalensis species group.

Key to the species groups of Charinus :

1. Female with thin, finger-like gonopods (Weygoldt 2005: figs 4,8).

.C. bengalensis species group (next key)

- Female with rounded, cushion-like gonopods (Weygoldt 2006: figs 1-10).

.C. australianus species group-

- Female with sucker-like gonopods (Vasconcelos et al. 2014: figs 17-18).

. C. brasilianus species group

Key to the Charinus species of the bengalensis group:

1. Basitiba IV divided into two pseudo-articles (Weygoldt et al. 2002: fig 12) .2

- Basitiba IV divided into three pseudo-articles (Delle Cave et al. 2009: fig. 3) .3

- Basitiba IV divided into four pseudo-articles (Weygoldt 2006: fig. 30) .4

2. Reduced lateral and median eyes, standard size legs, pedipalps held horizontally

. C. socotranus Weygoldt, Pohl & Polak, 2002

- No median and lateral eyes, elongate legs, pedipalps turned upwards .

. C. sty go chill obius Weygoldt & Van Damme, 2004

3. Female genitalia with curved, rigid finger-like appendage vestiges; genital operculum with pointed

apex; eyes well developed. C. bengalensis (Gravely, 1911)

- Female genitalia with straight, soft finger-like appendage vestiges; genital operculum with

curved apex; eyes well developed .C. pakistanus Weygoldt, 2005

- Female genitalia with straight, soft finger-like appendage vestiges; genital operculum

with straight apex; median eyes absent, vestiges of the lateral eyes .

. C. omanensis Delle Cave, Gardner & Weygoldt, 2009

4. Eyes well developed; female genital operculum with a steep ventral flexure at about two thirds

of its length; tibia I with 23 and tarsus I with 41 articles . C. africanus Hansen, 1921

- Median eyes, tubercle and lateral eyes present and prominent (Fig. 4B), frontal border of carapace

projected anteriorly (Fig. 4B), frontal process rhomboid (Fig. 4E), femur with five dorsal and

ventral spines; tibia I with 21 and tarsus I with 37 articles . C. ioanniticus (Kritscher, 1959)

MIRANDA G.S. et al. , New species and records of Charinus

- Median eyes extremely reduced and tubercle absent and lateral eyes extremely reduced (Fig. 4A),

frontal border of carapace rounded (Fig. 4 A), frontal process acute (Fig. 4C), femur with four dorsal

and ventral spines; tibia I with 21 and tarsus I with 37 articles. C israelensis sp. nov.

New localities of Charinus ioanniticus

During a biospeleological study in Israel, several specimens of C. ioanniticus were collected from man¬

made caves around the country, all of them new records for the species. The localities are: 1) Haruba

cave, central Israel; 2) several caves in Haifa city (along Carmel Mountain Ridge and along the Northern

Coastal Plain), northwestern Israel; 3) Khirbet Roma, Beit Netofa, north Israel (Fig. 6B). One of the

caves in Haifa (Al-’Atiqa cave) is particularly interesting as it is a man-made burial cave excavated in

kurkar sandstone, less than 200 m from the coastline. The cave is slightly below sea level (one of the

chambers is flooded with brackish water). This is, to our knowledge, the first record of a C. ioanniticus

populations living below sea level. Additionally, new findings were made in the city of Jerusalem, such

as in the entrance of the city (Lifta Tunnel) and in Rehavia (Metudela).

One additional new record is from the Yalan Dtiny a Cave (Beyrebucak Village, Gazipa§a District, Antalya

Province) in Turkey (Fig. 6A), a private, touristic cave which is being gradually destroyed by human

activities (A§an Baydemir et al. 2015). This record extends the known distribution of C. ioanniticus in

Turkey, despite being restricted to the southern region, close to the Mediterranean Sea.

Discussion

Charinus ioanniticus is a parthenogenetic and synanthropic species known from various localities in

East Mediterranean countries (Weygoldt 2005). It was described by Kritscher (1959) from Rhodos

Island, Greece, and later found in other Greek Islands (Weygoldt 1972), Israel (Kraus 1961; Rosin &

Shulov 1960), Turkey (Kovarik & Vlasta 1996; Weygoldt 2005; Seyyar & Demir 2007) and Egypt (El-

Hennawy 2002).

In Israel, Charinus ioanniticus is uncommon and usually encountered in man-made habitats, such as

the walls of old buildings and humid rooms. A similar distribution is also observed in the Caribbean

C. acosta (Quintero, 1983), another parthenogenetic species able to live in anthropic areas (Armas 2000;

Teruel 2011), and the Amazonian C. vulgaris Miranda & Giupponi, 2011, which is not found inside

buildings, but in secondary forests and scrapyards (Miranda & Giupponi 2011). Prior to this study, most

of the specimens from Israel were collected from a sewerage system in a single neighborhood in the

city of Jerusalem (Judaean Mountains, central Israel). A single specimen was also collected from an

archeological site (Sepphoris, Fig 6, Kraus 1961).

Like other Charinus species, C. ioanniticus inhabits places protected from direct sunlight and with

high humidity. In addition to dark man-made habitats, caves are perfect habitats for Charinus species

to occupy, and this environment can exert strong selective pressures, leading over time to speciation

events (Barr Jr. & Holsinger 1985). Species found in caves can have different ecological-evolutionary

specializations, being restricted to life in cavities (troglobites), or having strong affinities to caves but

being able to live outside them (troglophiles), or living in caves but being required to leave periodically

(trogloxenes) for various needs (Sleet 2008). Speciation in caves is a relatively fast event (Barr Jr. &

Holsinger 1985) that can happen under a variety of conditions, even when gene flow is present among

populations (Nosil 2008). Troglobite species usually have morphological adaptations such as reduction

or complete loss of vision and pigmentation, as well as elongation of appendages (Sket 2008; Trajano

2005). The morphological differences that arise in cave animals through time can fit in two main types

of changes: those that lead to the reduction of characters and those that improve characters (Klaus et al.

2013). Reductive and constructive traits tend to reduce costly traits (e.g., visual system, pigmentation)

European Journal of Taxonomy 234: 1-17 (2016)

(Riesch et al. 2011; Tan et al. 2005) and to enlarge certain functional features (e.g., leg and setae length),

respectively (Klaus et al. 2013).

Among all troglobite Charinus species known so far, only C. stygochthobius Weygoldt & van Damme,

2004 and C. troglobius have depigmentation of the body, elongated appendices and pedipalp spines, and

an almost complete absence of eyes. In the other species living in caves (e.g., C. eleonorae\ C. bordoni

Gonzalez-Sponga, 2002 and C. taboa Vasconcelos, Giupponi & Ferreira, 2016), those characters do

not occur simultaneously, showing that this set of features is rare within Amblypygi, even in species

considered troglobites or troglophiles. The new species of Charinus was found thus far solely in caves

in northern Israel, and has a pronounced reduction of the visual system. Although intensive searches for

other populations in the open and experiments with specimens outside the cave environment to assess

their survival capability were not done, we suggest that C. israelensis sp. nov. is a troglophile species.

Charinus israelensis sp. nov. belongs to the C. bengalensis species group, which includes C. africanus

Hansen, 1921, C. bengalensis , C. ioanniticus , C. omanensis Delle Cave, Gardner and Weygoldt 2009,

C. pakistanus , C. socotranus Weygoldt, Pohl and Polak, 2002 and C. stygochthobius. This group is

characterized by the finger-like female gonopods with a wrinkled and folded cushion base. Charinus

israelensis sp. nov. can be distinguished from C. africanus by the weakly developed median eyes, the

high number of pedipalp spines, the absence of the strong transverse flexure in the middle of the female

genital operculum and of the median elongation in the posterior border of the operculum (Weygoldt

2008), absence of flaps bent posteriorly over a small invagination in the tip of the finger-like process, by

the position of the trichobothrium be on distitibia IV, and by the number of articles in tibia and tarsus I.

Charinus israelensis sp. nov. differs from C. omanensis by the number and size of the pedipalp spines,

position of the trichobothrium be on distitibia IV, and development of the median eyes. It differs from

C. pakistanus by the absence of concave areas on the posterior margin of the genital operculum, the

position of the bifid tooth in relation to tooth II in the basal segment of the chelicerae, the high number

of basitibia IV articles (four in the new species and three in C. pakistanus ), the high number of articles

in tarsus I (37 in C. israelensis sp. nov. and 35 in C. pakistanus ) and the development of the median

eyes (weakly developed in C israelensis sp. nov. and well developed in C. pakistanus). Lastly, it differs

from C. stygochthobius by the absence of a small elongation in the middle of the genital operculum, the

position of the trichobothrium be on distitibia IV, the number and size of spines on the pedipalp and the

development of the median eyes.

Based on morphology, Weygoldt (2005) considered Charinus ioanniticus to be more closely related to

C. bengalensis and C. socotranus than to any other species. Consequently, C. israelensis sp. nov. is also

morphologically similar to those species. Charinus israelensis sp. nov. differs from C. bengalensis by

not having the genital operculum pointed posteriorly, the high number of teeth in the cheliceral claw,

the wealdy developed median eyes, and the high number of spines on the pedipalp; it differs from C.

socotranus by the shape of the genital operculum, the position of the trichobothrium be on distitibia IV,

and the number of pedipalp spines.

The new species differs from the closely related Charinus ioanniticus by the shape of the carapace

(Fig. 4A-B), the smaller number of pedipalp spines, the smaller size, and the acute shape of the frontal

process. The gonopods of C. israelensis sp. nov. and C. ioanniticus are very similar; as C. ioanniticus is

a parthenogenetic species (Weygoldt 2005), it could be that the new species has the same reproductive

strategy, which leads to reduced selective pressure on the genital region to modify it. Yet, additional non-

mutually exclusive explanations could be convergent evolution or recent differentiation. Live specimens

are being raised in the laboratory and the parthenogenesis hypothesis will be tested.

MIRANDA G.S. et al. , New species and records of Charinus

This is the first detailed description of a leg I of a Charinidae species and it is possible to note the

reduced number of sensilla when compared to the leg of Phrynidae and Phrynichidae (Delle Cave 1975;

Igehmmd 1987). The antenniform tarsus in the latter two families is covered with many sensilla (Beck &

Foelix 1974; Beck et al. 1977; Beck & Gorke 1974; Delle Cave 1975), and Igehmmd (1987) named the

different kinds of sensory structures as bristles, club sensilla, porous sensilla, rod sensilla, leaf-like hairs

(also called feather hairs), trichobothria, “pit organ”, “plate organ” and slit sense organs. C. israelensis

sp. nov. has only bristles, club sensilla and a modified claw. The lack of other sensory structures and

organs on leg I is interesting, since C. israelensis sp. nov. is possibly a troglobite species and, thus, relies

entirely on its sensory structures, but not on its vision, to find food and avoid predators.

Acknowledgements

We would like to thank Adriano Kury (MNRJ), Horweg Christoph (NHMW), Torenzo Prend ini

(AMNH), Peter Jager (SMF), Peter J. Schwendinger (MHNG) and Sarah Whitman (MZUF) for loan of

material. Nikolaj Scharff provided laboratory facilities and Hanne Espersen (both ZMUC) helped with

old and obscure literature. Yael Tubin kindly revised the English. We are also grateful to Kadir Bogac

Kunt for the donation of one specimen to ZMUC and for providing bibliography. Boaz Langford from

The Cave Research Unit, Shmulik Cohen from the Nature and Parks Authority in Israel, and Eran Levin,

Efraim Cohen and Igor Armiach assisted in locating and collecting specimens in the field. Avi Ben

Zaken, Boaz Zur, Segev Shalmon, Ori Segev and Nadav Biran contributed valuable information about

new localities of C. ioanniticus. Personnel at the SEM Platform Rudolf Barth (IOC-FIOCRUZ) - Roger

Magno Macedo Silva, Wendell Girard Dias and Romulo Custodio dos Santos - provided SEM facilities.

GSM thanks to the Coordenagao de Aperfeigoamento Pessoal de Nivel Superior (CAPES, Brazil) for

the Ph.D. Scholarship (Process number 8922-13-6). This study was supported by The Israel Taxonomy

Initiative (ITI) Biodiversity surveys grant, and by an ITI fellowship to SA. This is publication no. 902

of the Mitrani Department of Desert Ecology, Ben-Gurion University, Israel.

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Manuscript received: 19 February 2016

Manuscript accepted: 28 April 2016

Published on: 28 September 2016

Topic editor: Rudy Jocque

Desk editor: Kristiaan Hoedemakers

Printed versions of all papers are also deposited in the libraries of the institutes that are members of the

EJT consortium: Museum national d’Histoire naturelle, Paris, France; Botanic Garden Meise, Belgium;

Royal Museum for Central Africa, Tervuren, Belgium; Natural History Museum, London, United

Kingdom; Royal Belgian Institute of Natural Sciences, Brussels, Belgium; Natural History Museum of

Denmark, Copenhagen, Denmark; Naturalis Biodiversity Center, Leiden, the Netherlands.