Two new species and new records of Neanuridae ( Hexapoda : Collembola ) from Brazilian central Amazonia

Two new species of Neanuridae from the Amazon Rainforest of Northern Brazil are described and illustrated. The new species Friesea multiclavata sp. nov. (holotype male in MNRJ: Brazil, Amazonas State) belongs to the reducta-group and represents the first record of Frieseinae for Amazonas State in Brazil. Within Pseudachorutinae, the new species Furculanurida boiuna sp. nov. (holotype male in MNRJ: Brazil, Amazonas State) represents the third species of this genus without eyes and body pigment, together with Furculanurida africana (Massoud, 1963) – type species of the genus – and Furculanurida emucronata Zon et al., 2014, both from Ivory Coast, in Africa. Lastly, an indefinite species of Ectonura sp. (Neanurinae) is the second record of the genus for the Neotropical Region.


INTRODUCTION
Collembola has a worldwide distribution with a large number of species (Bellinger et al. 2018).Despite the several taxonomic contributions about springtails that have accumulated over the last years, there are few studies on the Brazilian fauna, which has resulted in vast areas lacking any springtail record (Abrantes et al. 2010, 2012, Zeppelini et al. 2018).In the state of Amazonas, for example, there are still several completely unexplored ecosystems for springtails (Abrantes et al. 2010(Abrantes et al. , 2012)).As for now, the Collembola fauna from the Amazon is second in terms of recorded species to the Atlantic Forest (Zeppelini et al. 2018).
Small river branches in the Amazon, known as 'Igarapés', are considered an important component of the forest.They provide an essential structural heterogeneity and sustain a highly diverse fauna.Their primary source of energy comes from organic matter from the riparian vegetation of adjacent forests (Lima andGascon 1999, Nessimian et al. 1998).
Neanuridae comprises six subfamilies, three of which occur in Brazil: Frieseinae, Neanurinae and Pseudachorutinae.
In this paper we describe, illustrate and provide diagnosis for two new species of Neanuridae of the genera Friesea and Furcu-lanurida.In addition, Ectonura, poorly known in the neotropics, is recorded for the first time in the Amazon, representing the second record for the Neotropical Region.The new species, Furculanurida boiuna sp.nov. is the third of the genus without eyes and pigment and the first with these characteristics found outside Ivory Coast, in Africa (type locality of the genus).Friesea multiclavata sp.nov., represents the first record of this genus for the state of Amazonas.

MATERIAL AND METHODS
Specimens were collected using trays, also known as yellow traps, placed upon soil litter found near Igarapés in five municipalities from central Amazon, Amazonas State.These trays, containing a mixture of water and detergent, were kept for 3-5 days and the captured fauna was sorted and mounted on glass slides, using Mark-André II as medium, and studied under optic microscope.
Abbreviations as follows: (AM)  Description.Body length: 0.51 mm (Holotype).Habitus cylindrical and robust, typical of Friesea.Color bluish-gray with ventral of head, legs and sternites white.Secondary granules moderately developed.Antennae shorter than cephalic diagonal.Ratio antenna: cephalic diagonal = 1: 1.4.Ant IV with apical bulb simple and subapically displaced on ventral side; subapical organite, dorsolateral S-microchaeta and 6 S-chaetae present dorsally (Fig. 1).Sensory organ of Ant III formed by five S-chaetae: two internal S-microchaetae bent externally and freely exposed; two subcylindrical guard S-chaetae and one smaller ventral S-microchaeta (Fig. 2).Ant I with 7 simple chaetae and Ant II with 11 chaetae, of which 10 are simple and one is strongly spatulate dorsoexternally (see detail in Fig. 7).
Head with 8+8 eyes in heavily pigmented eye-patch.Mandible strong with 5 unequal teeth; basal tooth measuring approximately twice the size of the others; maxilla head typical of the genus, with three lamellae; internal lamella with about 6 denticles (Fig. 3).Buccal cone short; Pre-labral/labral chaetae arranged according to the formula: 2/5,5,4.Labium typical of the genus, with papillated chaeta L, chaeta F about twice the length of E (Fig. 4).
Etymology.The specific name multiclavata is derived from Latin, meaning bearing nails, and is an allusion to the numerous clavate chaetae arranged along the tergites.
Remarks.Friesea multiclavata sp.nov.can be included in the reducta-group, which is composed of 14 species, according to Queiroz and Mendonça (2015), based on the following characters: 8+8 eyes and absence of furca and anal spines (Table 1).Despite the absence of anal spines, most species in this group, with the exception of Friesea africana Delamare Deboutteville, 1953, have some degree of chaetae modification on Abd VI.In this sense, the new species is unique within this group since it also presents modified chaetae on head and antennae.
Friesea multiclavata sp.nov. is very similar to Fr. albithorax Massoud & Thibaud, 1980 (Antilles) However, Fr. multiclavata sp.nov.has a simple apical bulb, 4,5,5 tenent hairs on tibiotarsi and ungues without teeth while Fr.lobulata has a trilobed apical bulb, only two clavate tenent hairs on legs I-III and toothed unguis.Friesea multiclavata sp.nov. is uniformly bluish-gray colored, while Fr.albithorax presents white thoracic tergites and the rest of the body is grey.Moreover, Fr. multiclavata sp.nov. is unique among the four species here referred, by the 10 strongly clavate chaetae on Abd VI, while the others have six (Fr.lobulata and Fr.mucumontana) or eight (Fr.albithorax) clavate chaetae.
Friesea multiclavata sp.nov.has an inconspicuous tegumentary protuberance on subcoxa I of legs I-III and ventrolaterally on Abd V (Fig. 7), also found in Fr. reducta and Fr.boitata.This structure was first mentioned by Massoud and Thibaud (1980) in specimens of Fr. reducta from Lesser Antilles.Later on, Fr. boitata was also found to possess the same structures on subcoxae I and Abd V.According to Queiroz and Mendonça (2015), it is possible that these structures were not mentioned in other descriptions as they may have not been properly visualized.
Although there are no phylogenetic studies for Neotropical species of Friesea, the proposition of a group relying on morphological similarities, such as reducta-group, represents the first step towards a better understanding of the genus' morphological diversity in the biogeographical region.As proposed by Queiroz and Mendonça (2015), it is possible to distinguish "subgroups" of species within this group based on the number of chaetae on Th I, being 2, 3 or 4 by half tergite.Despite that, we believe that the striking resemblance of these species, especially those previously mentioned with 2+2 chaetae on Th.I, suggests close relationship between them.
While further studies may clarify phylogenetic relationships, comparative morphological studies are still the mainframe for species recognition.In this sense, all described species in the mentioned subgroup can be distinguished mainly based on body chaetotaxy, especially chaetae morphology, such as clavate chaetae.This character is considered to be consistent and, therefore, it is widely used, especially for recently described species.
Etymology.The name of this species is a reference to the legendary Amazonian giant snake called Boiuna, in Amerindian *In part after illustrations and characterization of Fr. reducta by Massoud and Thibaud (1980).
Tupi Language.According to the legend, a huge snake grows to unrealistic proportions and, as it crawls through dry land, it leaves behind the grooves that later on become the Igarapés.
Remarks.The broadness and vagueness of the current diagnosis for Furculanurida was discussed in some studies involving species of this genus and its similarity to other genera (Thibaud and Palacios-Vargas 2000, Queiroz and Fernandes 2011, Zon et al. 2014).Recently, Zon et al. (2014) drew attention to the fact that Furculanurida has a poor definition, with many morphological features overlapping with the diagnosis of Pseudachorutes Tullberg, 1871 and Stachorutes Dallai, 1973 (see Table 2).The most conflicting aspects are related to number of eyes, PAO shape and number of vesicles and furcal development, as well as antennal chaetotaxy, more specifically the presence/ absence of dorsolateral S-microchaeta on Ant IV (Queiroz andFernandes 2011, Zon et al. 2014).Therefore, a revision of the genus is needed, along with a redescription of the type species, Fu. africana (Massoud, 1963).
According to Massoud (1967), Fu. africana has no eyes and no body pigments but has a well-developed furca.Regarding these characteristics, until now, Fu. emucronata Zon et al., 2014 was the only species similar to Fu. africana, except for the absence of mucro.In this sense, the new species Fu. boiuna sp.nov.represents the third in the genus without eyes and body pigment.
In relation to these three species, the most remarkable similarity among them is: the presence of a somewhat swollen branch of mandible and two basal strong teeth, although some minor differences can be observed in the total number of apical teeth.Furculanurida boiuna sp.nov., together with Fu. emucronata, has seven teeth on the and the ungues exhibit a tooth on their inner edge, while Fu.africana mandible has nine teeth and the ungues are devoid of teeth.Despite the mentioned similarities, Fu. boiuna sp.nov.shows a complete furca, while in Fu. emucronata it is incomplete, without mucro.Moreover, Fu. emucronata has 7 S-chaetae on Ant IV and between 13-16 vesicles on PAO of an elliptical shape, while Fu.boiuna sp.nov.shows 6 S-chaetae on Ant IV and 8-9 vesicles arranged in circular shape.
From a biogeographical point of view, the fact that the Neotropical Fu. boiuna sp.nov. is the first species outside of Africa with these set of characters is of considerable relevance.This indicates that a more widespread distribution, i.e. holotropical, is possible and raises questions regarding Pseudachorutinae distribution throughout the tropics.In this sense, despite their rareness, since few specimens are known from these three species, e.g., Fu. africana is known only by the holotype, these eyeless species are important for Pseudachorutinae taxonomy.
It must be highlighted that the new species clearly fits the recently proposed Arlesia-group of genera (Queiroz and Zeppelini 2017).Except for an elongated Sgd, almost subequal to Ant IV S-chaetae, Ant III-IV chaetotaxy is doubtlessly similar to the mentioned group of genera.For example Fu. boiuna sp.nov.has trilobed apical bulb; absence of ms; presence of S1-4, S8 and S10; x chaeta between a1 and i chaeta; and apically displaced Sgd.Regarding head and thorax chaetotaxy, the pattern similarity is also evident.On head: the reduced sd chaetae, absence of c row of chaetae, as well as only p1-3 chaeta on head.On thorax: Th.I with only 2+2 chaetae; Th.II and III with one dorsolateral chaeta posteriorly displaced.
In the same sense, according to original illustrations provided by Zon et al. (2014) for Fu.emucronata, it is possible to recognize one main chaetotaxal difference from the proposed Arlesia group: the absence of one dorsolateral chaeta on Th.II and III, probably the posteriorly displaced one.However, regarding all other chaetotaxy features of Ant III-IV (S10 is interpreted as S9 by Zon et al. 2014), head (sd with fewer chaetae -sd2-5?and c row absent) and tibiotarsi (although not drawn, M chaetae position is clearly basally displaced), it can also be placed inside the Arlesia group.
In short, as advocated by Queiroz and Fernandes (2011) and Zon et al. (2014), it should be reinforced that Furculanurida, now with 15 species (see Table 2), needs to be revised.We estimate that after such review, only these three species, Furculanurida boiuna sp.nov., Fu. emucronata and Fu.africana, would remain within the genus.However, further analyses must be made to stablish species relationships as well as their character evolution.
Remarks.Neanurinae includes seven tribes worldwide (Lobellini, Morulodini, Neanurini, Paranurini, Paleonurini and Sensillanurini) and is poorly known in the Neotropical region, with 75 recorded species -around 10% of a total of approximately 750 species.Only Paleonurini occurs in Brazil, with five genera and six species, Australonura gili Queiroz & Deharveng, 2014, Australonura neotropica Queiroz & Deharveng, 2014, Ectonura snowdeni, Itanura brasiliensis Arlé, 1959, Paleonura nuda Cassagnau & Oliveira, 1990and Pronura amazonica Cassagnau & Oliveira, 1990, the last two found in the Amazon Region (Zeppelini et al. 2018).Ectonura includes 17 species around the world, 11 of them from New Caledonia, five from South Africa and only one, Ectonura snowdeni, from mountains in the state of Minas Gerais, southeast Brazil.Moreover, the occurrence of Ectonura sp. from Australia was mentioned in an ecological work, but without a formal species description (Greenslade and Deharveng, 1990).A single specimen of Ectonura was found in a sample collected next to Amazonian Igarapés from Presidente Figueiredo municipality.Due to its poor state of conservation, only diagnostic characteristics for the genus level were identifiable, especially the central cephalic region with few tubercles and chaetal group arrangement.Despite being impossible to identify at species level, it still accounts for the second record of the genus for Neotropical Region and the first for the State of Amazonas, which implies a wider distribution within the tropics of the new world.

Table 2 .
Queiroz and Fernandes (2011) species of Furculanurida.Modified fromQueiroz and Fernandes (2011).Furculanurida duodecimoculata is the only species with 2+2 teeth on tenaculum, while the others show 3+3 teeth.The descriptions of Fu. africana, Fu. belemensis and Fu.goeldiana makes no reference to number of teeth on tenaculum. *