Rowlandius dumitrescoae species group: new diagnosis, key and description of new cave-dwelling species from Brazil (Schizomida, Hubbardiidae)

Abstract The Rowlandius dumitrescoae species group is reviewed and rediagnosed, and its composition is revised. The group now includes Rowlandius cousinensis, Rowlandius decui, Rowlandius dumitrescoae, Rowlandius insignis, Rowlandius linsduarte, Rowlandius monensis, Rowlandius peckorum, Rowlandius potiguar, Rowlandius sul, Rowlandius ubajara, and Rowlandius pedrosoi sp. n. A new species is described from a cave in northeast Brazil (Santa Quitéria, Ceará). Identification keys and distributional maps are provided for the species of the group. Sixteen species of Schizomida, including five of Rowlandius, are currently recognized from Brazil.


Introduction
Rowlandius Reddell & Cokendolpher, 1995, is the most diverse Neotropical genus of Schizomida with 63 described species (Reddell and Cokendolpher 1995;Teruel 2012;Teruel et al. 2012;Delgado-Santa and Armas 2013;Santos et al. 2013). Reddell and Cokendolpher (1995) proposed the genus with a broad concept, using characters that could also fit other genera, and was redefined by Teruel (2004). Reddell and Cokendolpher (1995) assumed Rowlandius as monophyletic, but this has never been tested in a phylogenetic analysis; on the contrary, the presence of several variable characters within the genus (e.g., the number of setae on the propeltidium and the shape of the spermathecae) indicates the opposite . Within Rowlandius, the biconourus species group was also proposed as monophyletic, but this hypothesis has not been tested either .
The species that compose Rowlandius were recognized as a species group long before the genus was erected, when almost all species of Schizomida were placed in Schizomus Cook, 1899 (the historical "trash can" of the order). The first attempt to subdivide Schizomus into species groups was made by Rowland and Reddell (1979a) who proposed seven; one of them, the dumitrescoae group, was divided in three complexes: dumitrescoae, primibiconourus and viridis complex. All Schizomus species of these complexes were transferred to Rowlandius by Reddell and Cokendolpher (1995). Later, new endeavors to detect and define groups within Rowlandius were made by Armas (2002), Teruel (2012) and Teruel et al. (2012), but these included only Cuban species and did not cover all morphological variation within the genus.
Almost 80% of Rowlandius species with a known male have striking secondary sexual dimorphism, i.e., the male pedipalp segments are much longer than that of the conspecific females. An interesting case of dimorphism is present in R. gracilis Teruel, 2004 andR. potiguar Santos, Ferreira &Buzzato, 2013, where the same population has both heteromorphic males with long pedipalp articles and homeomorphic males with shorter, female-sized pedipalp articles (Teruel 2004;Teruel et al. 2012;Santos et al. 2013;Oliveira and Ferreira 2014).
Rowlandius has an extensive geographic distribution, occurring from Cuba to Brazil. A major radiation of the genus seems to have occurred in the Greater Antilles, where the vast majority of the known species are found (Harvey 2003). In contrast, only five species have been described so far from continental South America (R. arduus Armas, Villarreal & Colmenares-García, 2009, R. linsduarte Santos, Dias, Brescovit & Santos, 2008, R. potiguar Santos, Ferreira & Buzzato, 2013, R. sul Cokendolpher & Reddell, 2000and R. ubajara Santos, Ferreira & Buzzato, 2013. The genus has been recorded from different biomes, including the Brazilian Amazonia, the Brazilian Atlantic forest, and the Venezuelan cloud forest (Santos et al. 2008;Armas et al. 2009). Recently, some species were discovered inhabiting caves or patches of forest inserted in dry areas of Brazil, the Caatinga (Santos et al. 2008;Santos et al. 2013).
In the present article, a new species of Rowlandius is described and illustrated from the state of Ceará, northeast Brazil. Additionally, the Rowlandius dumitrescoae group is rediagnosed, an identification key to its species is provided, and the relationships of the new species are discussed.
The keys were built based on the material analyzed and the original descriptions (in the case of species with no specimens available for examination). Males are unknown for Rowlandius sul and this species was not included in the male key. The preparation and illustrations of the spermathecae follow Villarreal et al. (2016). Dorsal, ventral, and lateral photos were made with a Leica MZ16 microscope attached to a FujiFilm X10 camera. Pictures of live specimens (courtesy of Denis Rafael Pedroso; Fig. 8) were taken with a Canon Power-Shot SX130 IS. To generate the SEM images, the specimens were critical point dried and mounted on stubs using an adhesive copper aluminum tape. The mounted stubs were then coated with platinum-palladium and scanned with a JEOL JSM-6390 LV.
Acronyms used: AMN anterior median notch of the chitinized arch; Dm dorso-median setae of abdomen and flagellum; Dl dorso-lateral setae of the abdomen and flagellum; LL lateral lobe of spermathecae; ML median lobe of spermathecae; Msp microsetae patch of the male flagellum; Vl ventro-lateral setae of the abdomen and flagellum.
Etymology. The species name is in honor of arachnologist Denis Rafael Pedroso, friend and collector of the type series (of this and many other new species of arachnids).
Prosoma (Fig. 1). Anterior process of propeltidium with two setae (one behind the other) followed by two pairs of dorsosubmedian transversally oriented setae; eyespot suboval; metapeltidium divided. Anterior sternum with 11+2 setae and posterior sternum with 5 setae. Anterior process as wide as long, with a wide base, narrowing abruptly, forming an almost right triangle; the tip of the process is curved downwards.
Opisthosoma (Fig. 1). Setae: Tergite I with two pairs of anterior microsetae and one pair of large Dm setae. Tergite II with three pairs of anterior microsetae parallel to each other, and one large pair of Dm setae. Tergites III-IX and XII each with one pair of large Dm setae; VIII with small Dl2; IX without Dm, but pairs Dl1 and Dl2 present; X without dorsal setae; XI with Dl1 and without Dl2; XII with short rounded posterodorsal process and with setae Dl1 and Dl2. Abdominal apodemes with coloration identical to the rest of the sternites. Sternites I-II with many scattered microsetae. Sternite  Flagellum (Fig. 2). In dorsal view flagellum diamond shaped, as wide as long, with rounded lateral and apical tips; with three bulges: a pair positioned dorsosubmedian (each bulge seated on opposite sides), without setae, separated by a depression, and one bulge in the central distal region (posteromedian), with the setae Dm4 on its apex; the central distal bulge is not connected to the lateral ones, with a depression between them. Dm1 is exactly on the edge between the diamond-shaped part and the stalk. Dl3 is positioned distally in relation to Dm4. Ventrally, Vm5 is closer to Vl2 than to Vl1 and Vm4. Vm1 is closer to Vm4 than to Vm2. Three microsetae on the lateral of the flagellum (msp), between the pairs Dl2/Vl1 and Dl3/Vl2, closer to the latter. Dl1, Vl1 and Vl2 forming a straight line in the frontal axis.  Chelicerae ( Fig. 3A-C). Movable finger sharp and curved; serrula with 16 hyaline teeth increasing in size towards distal region; guard tooth rounded. Lamella smooth. Fixed finger with bifid basal tooth, followed by four small subequal teeth; last tooth is the biggest, recurved, with an acute apex, subequal to the basal cusp of bifid tooth. Setation: G1 (setae group 1) with 3 spatulate setae; G2 with 4 feathered setae; G3 with 4 setae, all feathered dorsally and with serrated ventral surfaces; G4 with 2 setae, smooth, short and thick with thin apex; G5A with 6 similar sized feathered setae; G5B with 9 setae larger than G5A; G6 with 1 smooth setae longer than half of movable finger length; G7 with 6 setae decreasing in size from proximal to distal, feathered from the middle to its end. Setal group formula: 3-4-4-2-6-9-1-6.
Pedipalp (Figs 3D-E, 4). All segments without spinose setae. Trochanter: subcylindrical in α-heteromorphic males (in lateral view), longer than wide, with apical portion curved upward; short trapezoid in β-heteromorphic males and even shorter in females (Fig. 5); without apical spur (frontal projection); one ventral row of eight large setae with an intermediate row of three small setae. Femur: subcylindrical, club-shaped, with distal portion two times wider than the basal part; in α-heteromorphic males the femur is longer than the total length of the prosoma (pro-, meso-and metapeltidium together); in α-heteromorphic males the femur is longer than the patella (in β-heteromorphic males the femur and patella are subequal and in females the patella is longer); with few setae, only one ventral and one dorsal row of setae; on the ectal surface only one apical setae; on the mesal surface, one row of three setae. Patella: subcylindrical, club-shaped, with distal portion two times wider than the basal part; more setae than the femur, with two dorsal and two ventral rows, and four setae on the ectal surface. Tibia: cylindrical, α-heteromorphic males with distal portion slightly wider; shorter than half the length of  the femur and patella; in β-heteromorphic males and females, the tibia, femur and the patella have similar length. The tibia has the largest number of setae on the pedipalps, with some feather-like setae on the ventral region. Tarsus: conical, shorter than the tibia, with lots of setae in the distal third, with two dorsolateral and two ventrolateral   rows of setae; two ventrodistal spines pointing forward; tarsal claw sharp and curved, slightly larger than half the tibia length; tarsal spur present.
Spermathecae of paratype (Fig. 7). Two pairs of lobes; stalk of the lateral lobe (LL) long, curved (the tips close to each other) and very light colored (almost transparent); with few granules along the structure. Tip of the LL with a wrinkled, rounded structure (resembling a walnut), brown colored (which means it is sclerotized), of about half width of the stalk. The bases of LLs are separated by a distance similar to their lengths. The median lobes (ML) are short, cone-shaped, with a wide base and thin apex; its length is less than a third the size of the LL stalk; the integument is wrinkled with folds on its surface. Bases of the two lobes in contact. The chitinized arch is wider than long, cordiform (or as a "V", as described by Santos et al. 2013), similar to R. potiguar, however, in R. pedrosoi sp. n. the arch is strongly flattened. In R. potiguar, the vertex of the "V" has about 90-100° (a right angle tending towards the obtuse); in R. pedrosoi sp. n. the same vertex is clearly more obtuse than 150°. Distribution (Fig. 9). Only known from the type locality: Brazil, Ceará, Santa Quitéria. Natural history. The type locality is the largest cave in the state of Ceará, formed as a sloping crack (Fig. 8A-B) and with no more than seven square meters of floor space. The specimens were found in one of the few spots with some moisture in the ground. The soil was composed of damp earth of fine sediment agglomerated with gravel, small stones, shells of gastropods and bones from small mammals (Fig. 8C-F). When captured, the schizomids were walking on stones, gravel and debris, where the light barely reached (twilight zone).
Noteworthy of mention is a rare find of a secondary capilliconidium of a (probable) Basidiobolus sp. fungus among the cheliceral G7 setae (Fig. 3C, arrow; cf Blackwell and Malloch (1989)). The capilliconidium produces an apical droplet of extracellular material that helps the fungus to attach to and disperse with the host (Dykstra and Bradley-Kerr 1994). -Posterodorsal process on abdominal segment XII longer than wide (Fig. 6); base of the flagellum dorsal projections connected, i.e. without the median projection between them (Fig. 2)

Discussion
In general, species groups facilitate comparisons and identifications in speciose genera as they comprise a subset of a genus, and make the process of understanding relationships Table 1. Species groups and complexes proposed by Rowland and Reddell (1979a) and Reddell and Cokendolpher (1995) to the dumitrescoae group (when the species were still in Schizomus (R&R79) and after being transferred to Rowlandius (R&C95)).  (Passos et al. 2015). Initially, only few genera were recognized in Schizomida and some of these (e.g., Schizomus Cook, 1899; Trithyreus Kraepelin, 1899) accumulated a number of species, but eventually they were subdivided, first into species groups, some of which were later recognized as new genera (Rowland and Reddell 1979a, b, 1980, 1981. The dumitrescoae group is an example of species group that was raised to genus. The group was defined by Rowland and Reddell (1979a) and was later transferred to Rowlandius by Reddell and Cokendolpher (1995). At that time, all species were from Central America (see Table 1 and Fig. 9) and were defined by the large body size, carapace with two to four pairs of dorsal and one pair of apical setae, female flagellum with four flagellomeres, spermathecae elongated laterally and reduced in the middle, and a few other characters (Rowland and Reddell 1979a). Afterwards, Armas (2002) proposed other species groups based on Cuban species and defined them using mainly characters of the pedipalp and the spermathecae ( Table 2). Studies on South American Schizomida revealed Rowlandius species inhabiting Brazil (Cokendolpher and Reddell 2000;Santos et al. 2008;Santos et al. 2013) and those species have a set of characters shared with some Caribbean (R. cousinensis, R. decui, R. insignis, R. monensis and R. peckorum) and Central American species (R. dumitrescoae), suggesting that the Brazilian Rowlandius fauna also belong to the dumitrescoae group. The characters present in all these species are: 1) female spermathecae with long lateral lobes and with a broad distal expansion, 2) median lobes short, digitiform without distal expansion, 3) gonopod absent, 4) chitinized arch with opened anterior branch (without AMN) and posterior branch rounded (R. cousinensis, R. dumitrescoae, R. insignis, R. monensis and R. peckorum), or anterior branch closed and posterior branch retrocurved (R. pedrosoi sp. n. and R. potiguar) or rounded (R. linsduarte, R. ubajara and R. sul), 5) males with pedipalp elongated (such as R. decui, R. dumitrescoae, R. insignis, R. potiguar and R. pedrosoi sp. n.), and 6) male flagellum never trilobate in dorsal view, but diamond-shaped and with dorsal projection (absent in R. dumitrescoae and reduced in R. decui). Santos et al. (2008) already noted that R. linsduarte and R. sul are more closely related to each other than to any other species based on the female genitalia, but did not include them in any group. Here a new composition of the dumitrescoae group is proposed based on the above-mentioned characters (see also Table 4).

Group
Some Rowlandius illustrated in the literature are potentially part of the dumitrescoae group, but are not presently included, once no material was accessible during the preparation of the work. One of them is an undescribed species from Tortuguero,  . 3D); the spermathecae of the specimen fits the present definition of the dumitrescoae group, but as the species was not formally described and the male is not known, the correct relationship of the morphospecies cannot be assured by now. Another species that can potentially be part of the group is R. viridis; Rowland and Reddell (1979a) illustrated this species from four localities, and one of them (from Pedro Great Cave, Clarindon Parish) is similar to the standard shape of the dumitrescoae group, but since there is a huge variation in the size and shape of the lobes in this species, further studies are needed before reaching a conclusion on those populations. An interesting character observed in some species of Rowlandius (e.g. R. dumitrescoae, R. insignis, R. potiguar and R. pedrosoi sp. n.) is the strong sexual dimorphism of the palps. The femur and patella of the pedipalps are extremely long in α-heteromorphic males compared to females and homeomorphic males, as reported by Santos et al. (2013). Other cases of elongated male-dimorphic appendages in arachnids are found in harvestmen (Orrico and Kury 2009;Buzatto et al. 2011;Zatz et al. 2011) and whip spiders (Vasconcelos et al. 2014). It is possible that the elongate pedipalps of R. pedrosoi sp. n. evolved due to sexual selection pressures, similarly to that found in R. potiguar (Santos et al. 2013).
Rowlandius is the only short-tailed whip scorpion genus found in the dry biome of Caatinga (Santos et al. 2008;Santos et al. 2013). The four schizomid species found in that harsh environment (R. linsduarte, R. pedrosoi sp. n., R. potiguar and R. ubajara) are restricted to protected places, such as forests or caves, where the temperature is mild, the humidity is high and the variation these environmental conditions is lower. These species appear to be limited to these hypogean habitats, but they do not have apparent troglomorphisms and their presence in caves may be a recent invasion after climate change in Northeastern Brazil and retraction of the forest (Santos et al. 2007). The small size and the relatively thin cuticle of schizomids makes them sensitive to dehydration and caves serve as a suitable habitat for these animals (Oliveira and Ferreira 2014). The exotic species Stenochrus portoricensis Chamberlim, 1922, for example, has already been found in caves in Central Brazil (Gallão et al. 2015).