Synthesis of the Brazilian Poduromorpha (Collembola: Hexapoda) with Special Emphasis on the Equatorial Oceanic Islands

Simple Summary Endemic Collembola species are bioindicators of environmental quality since native species abundance is particularly sensitive to environmental disturbances. Oceanic island biota generally present high percentages of endemic species, and the vulnerability of these species is higher than those of the continents. The objective of this work was to carry out a survey of the Collembola species of the order Poduromorpha in the Brazilian oceanic islands and synthesize a distribution list of this order for Brazil. Our results reveal four new species of Collembola Poduromorpha for Brazilian oceanic islands that may be useful for the conservation strategies of these island regions and a contributor to the knowledge of the order in Brazil. Abstract We present new species and records of Poduromorpha for the Brazilian oceanic islands and synthesis of this order in Brazil. Friesea noronhaensis sp. nov., Friesea rochedoensis sp. nov., Willemia insularum sp. nov. and Paraxenylla zeliae sp. nov. are described and a diagnosis of the morphospecies Acherontiella sp. Lima and Zeppelini 2015 is provided. We present comparative tables, distribution and taxonomic keys of the Friesea, Arlesia, Brachystomella, Acherontiella, Paraxenylla, Xenylla, and Willemia found in the Brazilian oceanic islands and their respective congeners recorded in Brazil.


Introduction
The order Poduromorpha Börner, 1913 is represented by Collembola with an elongated body, thorax with three separate segments and prothorax with chaetae. Members of this order, about 3400 species, occur in all zoogeographic regions [1].
Abrantes et al. [2] summarized a list of Brazilian Collembola with 102 species of Poduromorpha and 2 morphospecies (Mesogastrura cf. ojcoviensis and Mesaphorura sp. gr. atlantica), none of them recorded in Brazilian oceanic islands.
We present results of recent surveys of the Archipelago of São Pedro e São Paulo, Atol das Rocas (Rocas Atoll) and the taxonomic advances for Fernando de Noronha   ria, Di--dorsointernal group of chaetae, De--dorsoexternal group of chaetae, DL--dorsolateral group of chaetae, CRFS-UEPB--Coleção de Referência da Fauna de Solo-Universidade Estadual da Paraíba, IUCN--International Union for Conservation of Nature. Brazilian states abbreviations according to Table 1.

Results
The Brazilian Poduromorpha fauna is recorded in the following states and oceanic islands (Table 1).

Poduromorpha Survey of the Brazilian Equatorial Oceanic Islands
The Poduromorpha fauna of the Brazilian oceanic islands is represented by 9 species, as follows: 3.1.1. Neanuridae Börner, 1901 Friesea noronhaensis sp. nov. Lima

Results
The Brazilian Poduromorpha fauna is recorded in the following states and oceanic islands (Table 1).

Poduromorpha Survey of the Brazilian Equatorial Oceanic Islands
The Poduromorpha fauna of the Brazilian oceanic islands is represented by 9 species, as follows: 3.1.1. Neanuridae Börner, 1901 Friesea noronhaensis sp. nov. Lima  Description. Habitus typical of the genus. Color in ethanol dark gray. Body with secondary integuments. Body length average: 512 µm (n = 5); holotype measurements in Table 2.
Head and body chaetotaxy composed of slightly rugged acuminate ordinary chaetae. S-chaetae smooth, except on Th II-III in DL that are roughly blunt. S-chaetae measuring about twice the size of anterior ordinary chaetae in Th II-III and Abd I-IV. Abd V-VI with posterior strong rough, blunt chaetae longer than others of the body. Sensillar formula by half tergum: 022/11111 (Figures 3 and 5).
Distribution. Friesia rochedoensis sp. nov. is registered only for Belmont island of the São Pedro e São Paulo Archipelago. The specimens were collected from seabird guano deposits over rocks. For the congeners registered in Brazil, see Figure 11. Distribution. Friesia rochedoensis sp. nov. is registered only for Belmont island of the São Pedro e São Paulo Archipelago. The specimens were collected from seabird guano deposits over rocks. For the congeners registered in Brazil, see Figure 11.  Distribution. Friesia rochedoensis sp. nov. is registered only for Belmont island of the São Pedro e São Paulo Archipelago. The specimens were collected from seabird guano deposits over rocks. For the congeners registered in Brazil, see Figure 11.  Brazilian Occurrence. In Brazil, this species is widely distributed in the states PA, PE, PB, PI, MG and RJ [13] (Figure 12). In Brazilian oceanic island Arlesia albipes recorded only in Fernando de Noronha Archipelago on Fernando de Noronha Island (SF sites). The specimens were collected on superficial soil and leaf litter.
Biogeographic Distribution. Type locality of Arlesia albipes is Margarita Swamp, Canal Zone, collected by J. Zetek and I. Molino on June 28, 1923, in a termite mound near the base of a tree stump and deposited at U.S.N.M. # 40383. According to [1], this species has been found in the following biogeographic regions: Caribbean mainland (24a), Antillean and South Florida (24b), Venezuela and Guyana (25), Amazon (26), Northeast and Central Brazilian (27) and Andean (28). Neotropical species.
Remarks. The specimens found in the Fernando de Noronha Archipelago are in accordance with the original description [14] and updates [15,16]. Lima and Zeppelini [3] recorded as A. sp. nov. For comparisons between Arlesia species recorded in Brazil, see Table 4.
Brazilian Occurrence. In Brazil, this species is widely distributed in the states PA PB, PI, MG and RJ [13] (Figure 12). In Brazilian oceanic island Arlesia albipes recorded in Fernando de Noronha Archipelago on Fernando de Noronha Island (SF sites). The s imens were collected on superficial soil and leaf litter.  [1], this specie been found in the following biogeographic regions: Caribbean mainland (24a), Anti and South Florida (24b), Venezuela and Guyana (25), Amazon (26), Northeast and Ce Brazilian (27) and Andean (28). Neotropical species.
Remarks. The specimens found in the Fernando de Noronha Archipelago are i cordance with the original description [14] and updates [15,16]. Lima and Zeppelin  Brazilian Occurrence. In Brazilian oceanic island B. agrosa recorded in Fernando de Noronha Archipelago on Fernando de Noronha and Rata Island (SF, TF sites), the specimens were collected in superficial soil and leaf litter. In Brazil, this species is widely distributed and has been registered in the following states CE, BA, PI, PE, PB, RN, ES, SP and RJ [13] ( Figure 13).
Insects 2021, 12, x FOR PEER REVIEW 17   Biogeographic Distribution. The type locality of this species is Maricao, Puerto Rico, collected by M. Capriles, take on Road 27, at 120 m altitude. According to [1], this species has been found in the following biogeographic regions: Caribbean mainland (24a), Antillean and South Florida (24b), Venezuela and Guiana (25), Amazon (26), Northeast and Central Brazil (27). Neotropical species.
Remarks. In addition to the original description [17], several authors contributed to the description morphological of this taxon, such as: [18][19][20][21]. The specimens of B. agrosa examined agree with the above descriptions. For comparisons between Brachystomella species recorded in Brazil, see Table 5.  Table 4.
Remarks. Acherontiella sp. [3] is similar to Acherontiella candida (Delamare Deboutteville, 1952), A. colotlipana Palacios-Vargas and Thibaud, 1985 and A. kowalskiorum Weiner and Najt, 1998 by type of guard sensilla of the Ant III organ (ring-shaped) and number of sensilla in Ant IV (with 5 globular sensilla). Acherontiella sp. differs from these species by anterior labrum chaetae (spiniform versus thin and smooth). For comparisons between Acherontiela species recorded in Brazil, see Table 6.
Distribution. Acherontiella sp. was found only on Fernando de Noronha Island in the SF region. The specimen was collected in soil litter. Additional material is required in order to properly describe this potentially new species. For other congeners records in Brazil, see Figure 14.  Description. Habitus typical of the genus. Color in ethanol blue. Body length average: 690 µm (n = 10); holotype measurements as in Table 2. Body with short acuminate chaetae (7-9 µm). Macrochaetae and S-chaetae (14-18 µm) about twice the length of ordinary chaetae.
Antenna ( Figure 15A). Ant IV with 4 thick S-chaetae and a small S-microchaeta between the 3 S-chaetae of the external group. Subapical organ present ( Figure 15A). Apical bulb simple. Sensory organ of Ant III with 5 S-chaetae (2 small, S3 and S4, behind a fold of the integument, 2 longer guard chaetae S2 and S5, and one external microchaeta S1). Ant II-I with 11 and 7 chaetae, respectively. Thorax I with 3 + 3 to 4 + 4 dorsal chaetae. Dorsal chaetotaxy of head and Th in Figure  16a; m1 absent, m2 present on Th II-III as macrochaetae, ms on Th II not visualized.
Thorax I with 3 + 3 to 4 + 4 dorsal chaetae. Dorsal chaetotaxy of head and Th in Figure 16a; m1 absent, m2 present on Th II-III as macrochaetae, ms on Th II not visualized.
Dorsal chaetotaxy of abdomen as in Figure 16b. Axial S chaetae 44/44,443; m2 on Abd I-III and a1 on Abd V as macrochaetae. Abd VI dorsally with 5 + 5 chaetae, one posterior chaetae and 3 An microchaetae on the supra-anal valve.
Distribution. The new species was found on Atol das Rocas Island in the SF sites. The specimen was collected in sandy soil near the psammophile vegetation and seabird guano on rocks. For the congeners registered in Brazil, see Figure 18.
Body with short acuminate ordinary chaetae, some slightly longer. Sensory chaetae are lanceolate and longer than ordinary chaetae. Antennae are somewhat shorter than cephalic diagonal.
Dorsal chaetotaxy (Figures 20b and 22). S-chaetae per half tergum formula: 22/11111, in m7 and p4 position on Th II and III, in p4 position on abdominal I to IV and p2 position on Abd V. Sensilla p4 on Th II-Abd I easily differentiated from ordinary chaetae. Abd IV without m-row. With two anal spines on m1 position.
Etymology. An allusion for being the only new species of this study that occurs in two different island regions.
Remarks. Willemia insularum sp. nov. shares characteristics with the buddenbrocki-group species sensu D'Hese 2000 [23][24][25] by S-chaetae S4 and S7 of Ant IV both large, globular, placed in the cavity, and covered in part by tegumental fold and absence of a0 chaetae on the head. The new species presents apical vesicle, Abd V with S-chaetae in p2 position; 3 + 3 chaetae on Th I, presence of anal spines; Abd IV and V with S-chaetae lanceolate. The new species is similar to W. dhesei Bu, Potapov and Gao, 2012 (Shandong, Pacific coast of China), W. delamarei Prabhoo, 1971 (Indian region); W. antennomonstrum Bu, Potapov and Gao, 2012 (Hainan, South China). Willemia insularum sp. nov. differs from W. dhesei by chaetotaxy of Abd IV (without m-row versus m1 to m4 present) and postantennal organ (7-8 versus 5-6 vesicles). W. delamarei has a postantennal organ with 8-12 vesicles, S-chaetae absent in Th II and Abd I while the new species present postantennal organ with 7-8 vesicles and 2 S-chaetae in Th II (m7 and p4) and 1 in Abd I (p4). Willemia insularum sp. nov., can be easily distinguished from W. antennomonstrum by the sensory organ of Ant III usual for the genus versus 2 expanded and granulated guard sensilla. For other morphological comparisons between Willemia species recorded in Brazil, see Table 8.
Insects 2021, 12, x FOR PEER REVIEW 23 o Description. Habitus typical of the genus. Color in ethanol white. Tegumental gran lation fine and regular. Body length: 490 µm (n = 5); holotype measurements as in Table 2.
Body with short acuminate ordinary chaetae, some slightly longer. Sensory chae are lanceolate and longer than ordinary chaetae. Antennae are somewhat shorter than phalic diagonal.
Antenna (Figure 19). Ant IV with 4 (S1, S2, S8, S9) subcylindrical sensilla, 2 globu sensilla S7 and S4, hidden each in a separate cavity. Microsensillum (ms) set in the cav of S7 sensillum. Sensilla S2 and S9 hardly differentiated from ordinary chaetae, S1 and subcylindrical. Apical bulb small and oval, subapical organelle set in a deep cavity, rou dish. Sensorial organ of Ant III with 2 long guard chaetae, 2 long subcylindrical sensi 1 ventral microsensillum, and a large integumentary fold hiding 2 internal sensilla. An and I with 11 and 6 chaetae, respectively.    Dorsal chaetotaxy (Figures 20b and 22). S-chaetae per half tergum formula: 22/11111, in m7 and p4 position on Th II and III, in p4 position on abdominal I to IV and p2 position on Abd V. Sensilla p4 on Th II-Abd I easily differentiated from ordinary chaetae. Abd IV without m-row. With two anal spines on m1 position.
Ventral abdominal chaetotaxy is presented in Figure 23a. Sternum of Abd IV with 12 + 12 chaetae. Sternum of Abd II with a-row with 2 chaetae on each side (a3 present). Anal lobes with 16 + 16 chaetae (2 i, 3 hr, e and b absent). Ventral tube with 4 + 4 chaetae ( Figure  23b). Tita I, II and III with 12, 12, 11 chaetae. Unguis without teeth, empodial appendage vestigial (Figure 23c).  Etymology. An allusion for being the only new species of this study that occurs in two different island regions.

Species
Remarks. The specimens analyzed agree with descriptions by [28][29][30][31]. For other morphological comparisons between Xenylla species recorded in Brazil, see Table 9. In the oceanic islands, the species was found in great abundance on the island of Fernando de Noronha in the SF and TF sites.  Distribution: This species is known only in the sand beaches of the Fernando de Noronha Islands. Small body size (350 µm) of I. mucrospatulata indicates that it inhabits narrow passages among the grains of sand [32]. Interstitial Collembola looks like typical euedaphic species but is flexible and slender enough to be able to move between sand grains of small size without changing the pore architecture [33]. All specimens in this study were found in the sand at the intertidal zone (SB sites).
Remark. The specimens analyzed agree with the original description by [34]. For others, morphological comparisons between Isotogastrura species recorded in Brazil, see Table 10.

Species List of Brazilian Poduromorpha
In Brazil, Poduromorpha fauna is registered in 18 states and 3 oceanic islands (Table 11) Table 2. This number represents an increase of 41 new species records since the last synthesis by [2]. Table 11. Species of Poduromorpha recorded from Brazilian states and oceanic islands-updated from [2]. *-New record after [2]. In parentheses, information obtained from non-original reference. "?" following state abbreviation-questionable state record. "un"-unspecified or unknown Brazilian collection habitats. World distribution-see Methods/Species list of Brazilian Poduromorpha. "?" following the distribution abbreviation-questionable distribution record. Habitatrepresentative type of habitat for the species. "un"-unspecified or unknown habitat (Brazilian distribution, locality abbreviations refer to Brazilian states and Insular locality as listed in Table 1). Family names in bold.

Discussion
The first Collembola species registered in Brazil was the Seira musarum Ridley, 1890 (Entomobryomorpha), whose type locality is Fernando de Noronha. However, after this pioneering study, the only works with Collembola in Brazilian oceanic islands were the description of Isotogastrura mucrospatulata Palacios, Lima and Zeppelini 2012 [36] and the species survey done by Lima and Zeppelini, 2015 [3] both in Fernando de Noronha.
Our results show that Poduromorpha fauna of the oceanic islands showed a high percentage of species known only from their type localities and with a great potential for endemisms. All of the Poduromorpha species found in the São Pedro and São Paulo archipelago and Atoll das Rocas are undescribed and with consistent morphological differences in relation to the species found on the continent. Fernando de Noronha, the only Brazilian oceanic island where tourist visitation is allowed, one endemic (I. mucruspatulata), four with wide continental distribution and two new species described here. These results may be useful in the management and environmental monitoring programs of oceanic islands in Brazil.
Although the increase in the number of Brazilian Poduromorpha species over the past decade has been relevant (about 35% since [2]) when we consider the variety of Brazilian continental biomes and the complex physiognomy of these areas, current knowledge of the Poduromorpha fauna can still be considered scarce and far from providing a reliable overview of its biogeographical panorama.