A Survey of the Brazilian Dicranocentrus Schött (Collembola, Orchesellidae, Heteromurini) with the Description of a New Species and Notes on the Genus

Simple Summary Springtails (Collembola) are microarthropods commonly found in terrestrial habitats, especially associated to the soil. Dicranocentrus Schött is one of the most representative genera of the family Orchesellidae Börner of springtails, with 69 described species in tropical regions of the world. Here we describe a new Brazilian species of the genus, especially using data on its chaetotaxy, the comparative study of the shape and the arrangement of body chaetae. We also use such data to compare and better understand the morphology of other species of the genus, and to better recognize them using comparative tables and identification keys. Abstract Dicranocentrus Schött is the most diverse and widespread taxon of Neotropical Orchesellidae. In Brazil, the genus is represented by 11 species found in humid forested areas of Atlantic and Amazon forests domains. Here we describe in detail Dicranocentrus abestado sp. nov. from Chapada Diamantina, Caatinga domain, Brazil. The new species belongs to the marias group sensu Mari-Mutt, due to the absence of most posterior macrochaetae on the dorsal head, and resembles other Neotropical species with 3, 2 and 2 central macrochaetae on abdominal segments I–III. However, the new species is unique especially by its reduced colour pattern combined with its empodial complex morphology. We compare Dicranocentrus abestado sp. nov. with 27 other taxa from the New and Old World, including all species with 3 macrochaetae on the first abdominal segment; provide notes and details on the morphology of the compared species plus identification keys to Brazilian and all species of the genus with similar abdominal chaetotaxy. We also discuss the current taxonomical knowledge on Brazilian Dicranocentrus and provide notes on its chaetotaxy and Heteromurinae systematics.

Type species: Dicranocentrus gracilis Schött, 1893 [7] Remarks: The presence of rounded and/or truncate coarsely ciliate scales on body and appendages, sens and ms formulae of dorsal Th. II to Abd. III = 2,2| 1,3,3 and 1,0| 1,0,1, respectively, short Abd. IV (less than two times the length of the Abd. III at the midline) and bidentate mucro were suppressed from the genus diagnosis since they are suprageneric diagnostic features. The updated diagnosis changes the number of sensilla on Abd. V compared to previous literature, as in [2,14,15], due to the description of the new species. More details on Dicranocentrus overall morphology are presented in [12,14,15,[43][44][45].  Tables 2 and 3 with about 27 smooth chaetae. Tenaculum corpus with one rough chaeta. Manubrium with three and dens proximally with one dorsal smooth acuminate chaetae, manubrial plate with 10-12 ciliate chaetae plus two pseudopores, manubrium ventro-apical region with one ciliate chaeta. Dens with 16-20 spines distributed in 2-3 rows in proximo-internal region.
Description: Habitus typical of the genus (Figure 1). Body length (head + trunk) of holotype = 1.57 mm; range of type series length (adult specimens) = 1.48-1.72 mm; average body length of adult females = 1.59 mm; average body length of adult males = 1.51 mm; average body length of adults = 1.56 mm. Specimens fixed in ethanol with yellowish background, Ant. I distally and Ant. II-IV dark blue, frontal head (clypeal and anterior post-labial regions), lateral Th. I-III, dorsal Abd. VI, coxae (including epi and subcoxae), distal half of femurs and proximal 3/4 of tibiotarsi light blue (Figure 1). Coarsely ciliate scales present on Ant. I, Ant. IIa, head (dorsally and ventrally), dorsal trunk, legs (all segments), ventral tube anterior and posterior faces, ventral manubrium and ventral dens. Dorsal head and trunk mac, mes and mic ciliate.          Abdominal appendages ( Figure 6C-I): Ventral tube anterior face with about 17-19 ciliate chaetae, five mac and 12-14 slender chaetae with different sizes, distal region with one mac and two mes ( Figure 6C); posterior face with four unpaired (one very large) and 9-10 paired smooth chaetae with different sizes, plus 3-4 central ciliate chaetae (lateral side with many more ciliate chaetae, partially represented in Figure 6D); lateral flap with about 27 smooth chaetae, three clearly longer   /UFRN): two males,  one female and two juveniles, plus one female (INPA-CLL 0000114), same data as holotype.
Legs ( Figure 6A,B): Trochanteral organ with 22-27 spine-like smooth chaetae, 22 on holotype ( Figure 6A). Distal halves of tibiotarsi I-II with three and tibiotarsus III with five smooth chaetae on inner side, respectively. Tenent hairs discretely capitate or acuminate, two small pretarsal chaetae present, tibiotarsus III distal smooth chaeta subequal in length to tenant hair ( Figure 6B); empodial complex III ratio of smooth chaeta: tenent hair: unguiculus: unguis of holotype as 1:1:1.5:2.2. Ungues with an outer pair of lateral undeveloped teeth on proximal 1/4, inner side with four teeth: two paired basal teeth on proximal 1/3, one unpaired median tooth on proximal 3/5 with the same size of the basal teeth, and a minute apical tooth on distal 1/8 easily overlooked due to size and position; unguiculi lanceolate, leaf shaped, antero-internal lamella wide, all lamellae smooth except postero-external lamella with a large tooth on proximal 1/2 ( Figure 6B).
Etymology: "abestado" or "abestada" is a regional expression used in Northeastern Brazil which means "fool". The expression is commonly used between friends.
Habitat: The new species was found in Chapada Diamantina National Park, in the southern region of Caatinga phytogeographic domain, from moist rocky and sandy soil samples surrounded by forested areas. The climate of the area is "Aw" according to the Köppen-Geiger system-an equatorial climate with dry desert-like summer [46]. The specimens were collected at the beginning of the raining season. Table 2. Comparison among Dicranocentrus species of the marias group from the New Word with similar morphology (head S series with 7 mac, basomedian labial field with M1 chaeta ciliate, m2 and e smooth, papilla E lateral process short, Th. II without p5 mac and Abd. I-III with 3, 2 and 2 central mac, respectively).    Remarks: Dicranocentrus abestado sp. nov. belongs to the marias group of species as its dorsal head chaetotaxy is devoid of A1, S2 and all posterior mac except Pa5 and rarely Pp5 [12,47]. The new species is most similar to other Neotropical taxa from marias group, especially D. antillensis Mari-Mutt, 1979 [12], D. icelosmarias Soto-Adames and Anderson, 2017 [48], D. marias Wray, 1953 [49] and D. paramoensis Mari-Mutt, 1983 [47] since they also share seven mac on dorsal head S row (S0-1, S3-6), labial papilla E lateral process (l.p.) short, not reaching the apex of the papilla, labial basomedian field (labial triangle) with M1 chaeta ciliate and m2 and e smooth, Th. II lacking p5 mac and Abd. I-III with 3, 2 and 2 central mac, respectively. However, the new species can be readily separated from all others due to its colour pattern, with bluish pigments on thorax laterally to coxae, Abd. VI, distal femurs distally and all tibiotarsi (otherwise in the other species) and by its wide leaf-shaped unguiculus (normal in the other species), with one posterior tooth (absent in D. icelosmarias) ( Table 2). The new species also lacks Pp5 mac on dorsal head (present in D. paramoensis), labial basomedian field unscaled with R chaeta ciliate (with scales in D. antillensis, R chaeta smooth at least in D. icelosmarias and D. marias), 3 basal post-labial basal chaetae around the cephalic groove (2 in D. paramoensis), Th. II with 3 m4 and 4 p mac (2 and 5, respectively, in D. antillensis and D. paramoensis), Th. III with 3, 0, 3 mac on a, m and p rows, respectively (4, 1, 3 in D. antillensis and 2, 1, 3 in D. paramoensis), unguis minute apical tooth (absent in D. antillensis, D. icelosmarias and D. marias) and dorsal manubrium with 3 smooth acuminate chaetae (absent in D. antillensis, 4 in D. icelosmarias and D. paramoensis). A detailed comparison of the main diagnostic features among such species is presented in Table 2.

Species [References
Regarding the Brazilian species of Dicranocentrus, D. abestado sp. nov. is most similar to D. amazonicus, also from the marias group (Table 3). These species share similar colour patterns and dorsal head macrochaetotaxy, maxillary outer lobe basal chaeta acuminate, basomedian labial field unscaled with M1 chaeta ciliate, Th. II p row with four mac and Th. III a, m, p rows with 3, 0, 3 mac, respectively. However, the new species differs from D. amazonicus especially by labial chaeta R ciliate (smooth in D. amazonicus), Abd. II with 2 central mac (1 in D. amazonicus), Abd. III with 1 lateral mac (2 in D. amazonicus), Abd. IV with 4-5 central mac (3 in D. amazonicus), unguiculus wide with one posterior tooth (normal and toothless in D. amazonicus) and unguis with a minute apical tooth (absent in D. amazonicus). Dicranocentrus pikachu is the second previously known species of the marias group from Brazil; however, it is remarkably different from D. abestado sp. nov., especially as it has 17 dorsal head An mac (11-12 in the new species), maxillary outer lobe basal chaeta blunt (acuminate in the new species), Th. II with 5-6 p chaetae (4 in the new species), Th. III a, m, p rows with 5, 1, 3 mac, respectively (3, 0, 3 in the new species), Abd. I with 5 central mac (vs. 3), Abd. III with 2 lateral mac (vs. 1), unguis lacking the apical tooth (vs. present) and about 50 dental spines (vs. [16][17][18][19][20]. Among the Brazilian species, D. abestado sp. nov. is the only one with 3 mac on Abd. I (Table 3). Dicranocentrus heloisae typically has 5 mac on Abd. I [18]; however, it was reported in specimens also with 3 [21]. Here, we disregard such observations, since it is possible that specimens of D. heloisae with 3 mac on Abd. I represent another species, as the macrochaetatoxy of Abd. I is quite a stable feature in Dicranocentrus; or such specimens may represent juveniles. Even so, D. abestado sp. nov. also differs by head with 0-1 posterior mac (marias group), while in D. heloisae there are 2 (gracilis group). In addition, D. heloisae has a very distinct colour pattern, plus large number of chaetae in trochanteral organ and dental spines, compared to the new species. Further comparisons between both species and among other Brazilian taxa are presented in Table 3 and in the identification key in the discussion.

Brazilian Species of Dicranocentrus
The knowledge on Brazilian Dicranocentrus further increased during the past decade but is still limited at some level. With the description of D. abestado sp. nov. there are now 12 species of the genus recorded from Brazil (Table 1). Most of these species are only known from their type locality, with the exception of D. albicephalus (from Rio de Janeiro and Espírito Santo states), D. heloisae (from Rio de Janeiro, Espírito Santo, São Paulo, Minas Gerais and Bahia states) and D. silvestrii (Rio de Janeiro, Bahia and possibly Santa Catarina states) [4,[19][20][21][61][62][63]. Of such species only D. silvestrii was recorded in other countries and it is considered widespread in South America, known from Argentina, Bolivia, Brazil, Chile, Peru and Venezuela [9], although its records are doubtful (see comments on this species, below). There are also few records of unidentified morphospecies from Brazil, as in [62,64], which combined to the nominal species records suggest that Dicranoncentrus is widely distributed at least in the Atlantic and Amazon Forest domains, as well as humid forested areas within the Caatinga domain.
Concerning the morphology of Brazilian species, D. albicephalus, D. cuprum, D. heloisae, D. magnus, D. marimutti, D. melinus and D. pikachu were very well studied and described/redescribed by Xisto and Mendonça [18,20,21]. Very few diagnostic features are unknown to these species, such as the number of smooth chaetae on furca and trunk sens formula, for example. Unfortunately, the type/analysed material of such species was lost in the fire in the National Museum of Rio de Janeiro at the end of 2018. The description of Dicranocentrus amazonicus is succinct as to most species of the genus, and some diagnostic features are unknown or unclear to it, such as the presence and distribution of smooth chaetae on antennae, tibiotarsi and furca, trunk sens formula, antennal and ventral head chaetotaxy (except labial and maxillary outer lobe chaetotaxy), number of tenaculum chaetae, as well as other features. The labral papillae shape and position and absence of scales on ventral tube are also unlikely characters and should be better investigated in this species [17]. Nevertheless, there are enough data to separate this species from other Brazilian and Neotropical taxa (Tables 2 and 3). Dicranocentrus bicolor, D. termitophilus and D. silvestrii, however, are poorly described and their names cannot be used with confidence for now, as already stated by Mari-Mutt [12] and Xisto and Mendonça [21]. Because of this we considered the three species as species inquirendae.
Dicranocentrus bicolor was collected in the Blumenau municipality, Santa Catarina state, inside nests of Eutermes arenarius termites [13]. Even though the type material of this species is in poor condition [12], there are sufficient data on the type locality and morphology, such as colour pattern, empodial complex and proximal dens-See Table 3 and Handschin ( [13], pp. 23-24)-which allow for the collection of fresh samples, recognition of the species and its redescription. Dicranocentrus termitophilus-type material is also in poor condition [12], but the two type specimens were collected from Minas Gerais state-wrongly spelled "Minas Gueras" by Handschin [13]-inside nests of Cornitermes similis termites. Minas Gerais is the fourth largest state in Brazil with an area of about 586,500 square kilometres and encompass three very distinct biomes: Atlantic Forest (a tropical rainforest); Caatinga (a semi-arid landscape covered by a mosaic of very different phytophysiognomies) and Cerrado (a savanna-like domain). However, the few details on D. termitophilus morphology-see Table 3 and Handschin ([13], pp. 25-26)-the overall affinity of Brazilian Dicranocentrus species for humid forested areas (Table 1) and the biological association, even if accidental, with Cornitermes similis may provide enough data for the collection of new samples and the redescription of D. termitophilus. The very brief and generic description of D. silvestrii by Absolon ([24], pp. 105-106) makes it impossible to clearly separate this species from most taxa, and so we excluded it from Table 3. For instance, the body colour is described as yellowish, but also as dark in one species variation, without further details. Absolon's description also reports a capitate tenent hair (seen in several species of the genus and in a few polymorphic ones, as shown in Tables 2-5) and unguiculus with a medial tooth (also seen in several species, as shown in Tables 2-5). However, the most obscure data for this species is its type locality, which is listed only as "in South America" ( [24], p. 106). Since its type material is apparently lost [12], the real type locality is unknown and none of the posterior descriptions consulted the type material [65,66], the name D. silvestrii is highly dubious and should not be used in any case. One last detail about this species is the record of Börner [4] to D. silvestrii on orchids from "São Francisco", Brazil. This locality is as dubious as the species name, since "São Francisco" could represent several different localities far apart in Brazil. Further details on this issue are discussed in ( [67], pp. 161).

Notes on Dicranoncentrus Chaetotaxy
Dicranocentrus species morphology is widely variable as partially represented in Tables 2-5. Dorsal head macrochaetotaxy can have, among other chaetae, S2, S6i and several posterior mac (on Pa, Pm and Pp rows) or can be devoid of at least some of these mac [12]. Trunk dorsal macrochaetotaxy of most species has few or none secondary mac, other than those on the Th. II anterior collar, m4 and p groups, and m3e on Abd. II, but differences in the presence and number of some primary mac or their multiples occur. Such data are of taxonomic relevance, especially on Th. II-III and Abd. I [12]. The number and displacement of smooth acuminate chaetae on proximal antennae, tibiotarsi, manubrium and proximal dens are of specific value, as well as the presence, number and position of dental spines. Labial basomedian field M and R chaetae multiples, which can include scales on some species, are so inconstant and can be so abundant that in some cases can prevent a clear understanding of which are some of the primary chaetae. Even the tenaculum corpus chaetotaxy diverges among the species (and can be polymorphic in few ones), as represented in Tables 4 and 5. Such variations among the species plus our finding of D. abestado sp. nov. with an unexpected number of seven sens on Abd. V (previously known as only four, but unknown to most taxa) may point out to an artificial status for Dicranocentrus. For instance, Sinodicranocentrus Zhang, 2020 [15] was recently erected based especially on ungual morphology and Abd. V S-chaetotaxy, and it was supported by molecular data; otherwise Dicranocentrus would be paraphyletic ( [15], p. 15, Figure 1). In this sense it is possible that the widely variable morphology of Dicranocentrus may hide more distinct lineages of Heteromurini, and further studies on its morphology and systematics may unveil this condition. This approach could also confirm/refute Mari-Mutt's groups of species [12].

Notes on Dicranocentrus Species Groups and Related Genera
Mari-Mutt's groups of species based on dorsal head macrochaetatoxy are quite useful for the current taxonomy of Dicranocentrus [12,17,18,20,21,41,57]. Distribution endorses Mari-Mutt's groups at some level [12] (as partially represented in Figure 7). For instance, the marias group is almost exclusively Neotropical, with the exception of D. spinosus Prabhoo, 1971 [68] described from India. This group is well delimited by the reduction in dorsal head macrochaetotaxy, devoid of S2 and most post-occipital mac, aside from Pa5 (which can be rarely absent as well) and Pp5 (only seen in D. paramoensis) [12].

Brazilian Species of Dicranocentrus
The knowledge on Brazilian Dicranocentrus further increased during the past decade but is still limited at some level. With the description of D. abestado sp. nov. there are now 12 species of the genus recorded from Brazil (Table 1). Most of these species are only known from their type locality, with the exception of D. albicephalus (from Rio de Janeiro and Espírito Santo states), D. heloisae (from Rio de Janeiro, Espírito Santo, São Paulo, Minas Gerais and Bahia states) and D. silvestrii (Rio de Janeiro, Bahia and possibly Santa Catarina states) [4,[19][20][21][61][62][63]. Of such species only D. silvestrii was recorded in other countries and it is considered widespread in South America, known from Argentina, Bolivia, Brazil, Chile, Peru and Venezuela [9], although its records are doubtful (see comments on this species, below). There are also few records of unidentified morphospecies from Brazil, as in [62,64], which combined to the nominal species records suggest that Dicranoncentrus is widely distributed at least in the Atlantic and Amazon Forest domains, as well as humid forested areas within the Caatinga domain.
Concerning the morphology of Brazilian species, D. albicephalus, D. cuprum, D. heloisae, D. magnus, D. marimutti, D. melinus and D. pikachu were very well studied and described/redescribed by Xisto and Mendonça [18,20,21]. Very few diagnostic features are unknown to these species, such as the number of smooth chaetae on furca and trunk sens formula, for example. Unfortunately, the type/analysed material of such species was lost in the fire in the National Museum of Rio de Janeiro at the end of 2018. The description of Dicranocentrus amazonicus is succinct as to most species of the genus, and some diagnostic features are unknown or unclear to it, such as the presence and distribution of smooth chaetae on antennae, tibiotarsi and furca, trunk sens formula, antennal and ventral head chaetotaxy (except labial and maxillary outer lobe chaetotaxy), number of tenaculum chaetae, as well as other features. The labral papillae shape and position and absence of scales on ventral tube are also unlikely characters and should be better investigated in this species [17]. Nevertheless, there are enough data to separate this species from other Brazilian and Neotropical The gracilis and sundanensis groups are characterized by a more complex dorsal head macrochaetotaxy, with post-occipital series with two or more mac, but they differ from each other by the presence (sundanensis) or absence (gracilis) of S2 mac. Other morphological features of both are mixed and should be better investigated since they raise doubts if the gracilis and sundanensis groups are really independent taxa. For example, both groups hold species with one or two central mac on Abd. III, with or without dental spines, and with or without a very peculiar proximal blunt mac on dorsal dens, described to South Asian species as D. janetscheki Yosii, 1971 [69], D. indicus and D. javanus, from the sundanensis group, and D. fraternus Mari-Mutt and Bhattacharjee, 1980 [53], from the gracilis group [53,56,60,69]. The head chaetotaxy of D. janetscheki and D. indicus are unknown, and thus it is not entirely clear if they really belong to the sundanensis group [12,69]; D. javanus, however, belong to that group [56].
The presence of 1 proximal dental mac was also reported to Falcomurus chilikaensis Mandal, 2018 [70] (Heteromurini), the sole species of the genus described from India. This species was compared specially with Heteromurus due to the presence of only Ant. I subdivided (so, with five antennal segments) and Abd. I devoid of mac [70]. However, there are incongruences on this species description [15], which may point to an inaccurate interpretation of Abd. I chaetotaxy as well. Additionally, Dicranocentrus specimens can rarely have four or five antennal segments, as juveniles or when the antennae are regenerating [12]. Finally, among the Orchesellidae, only species of Dicranocentrus and now Falcomurus have a proximal dental mac. Because of this, it is possible that Falcomurus represents a Dicranocentrus species.
Mari-Mutt's phylogeny suggested the marias and gracilis groups had a close ancestral link [12]. Due to the wide Pantropical distribution of the gracilis group [3,12], it is possible it was already established at least during the Jurassic (about 180 mya), and the marias group emerged from a gracilis-like ancestor after the brake of western Gondwana in the Neotropical Region. In this sense, the presence of D. spinosus of the marias group in India was possibly due to: (1) human-mediated dispersal events, such as plant and soil carrying during the past five centuries; (2) it emerged independently from the Neotropical marias group, and its resemblance with other taxa is due to convergence. Mari-Mutt's phylogeny also suggested that the sundanensis group and Pseudodicranocentrus Mari-Mutt, 1981 [45] (formerly Dicranocentrus circulatus group) are closely related [12]. The distribution of the sundanensis group is Oriental to Australasian (as partially represented in Figure 7), while Pseudodicranocentrus is endemic to Mexico and Guatemala [3,9,45]. If Mari-Mutt's hypothesis is correct, the presence of Pseudodicranocentrus in Central America possibly occurred by the dispersal of its ancestor by the Pacific Ocean, similarly to the model of Christiansen and Bellinger for the Hawaiin colonization [71].
Below, we provide an identification key to all species of Dicranocentrus with 3 mac on Abd. I. They belong to marias, sundanensis and gracilis groups. Further data on such species are presented in the remarks on the new species and in Tables 2, 4 and 5.
-Labial basomedian field r chaeta smooth; ungues devoid of apical tooth; unguiculi normal . . . 8. Head sutural series with 7 mac (S2 absent, Figure 2F) . . . (gracilis group) 9 Abd. IV and a postantennal organ (seen only in Alloscopus among the Heteromurinae, variable among other Orchesellidae), such features should be interpreted as plesiomorphies, as well as the presence of hook-like labral papillae and tenaculum with more than one chaeta, also seen in some of their species. In this context, if we consider the alternative hypothesis to Entomobryoidea topology as Orchesellidae + (Heteromurinae + Entomobryidae/Paronellidae), the presence of scales could be the synapomorphy of the more derived Entomobryoidea, including Heteromurinae, and it was secondarily lost possibly more than one time among the Entomobryinae [75,76]. To support this interpretation, the basal Entomobryinae and all Seirinae also share coarsely ciliate scales with the Heteromurinae [72,75,77].

Conclusions
After the description of Dicranocentrus abestado sp. nov. there are now 12 species of the genus recorded from Brazil. Its Abd. V S-chaetotaxy with seven sens, unmatched in the genus, combined with the widely variable morphology of Dicranocentrus species, and the recent description of Sinodicranocentrus based on ungual morphology and S-chaetotaxy raises doubts about the validity of the former genus. Regarding the Brazilian species inquirendae, there is arguably enough data for the collection of fresh specimens of D. bicolor and D. termitophilus and their redescription. Conversely, D. silvestrii identity, including its real type locality, remains obscure and such a name cannot be used with certainty. The Heteromurinae position within Entomobryoidea remains puzzling, but the morphology, especially the presence of scales, may indicate its affinities with more derived taxa than the unscaled Orchesellidae.