New species of Nothobrya (Collembola: Entomobryidae) from Southeast Brazil

ABSTRACT

The collembolan family Entomobryidae, one of the most numerous, diverse and widely distributed, was recently reviewed in a work that integrated molecular and morphological characters. The new classification includes seven subfamilies, one of which, Nothobryinae, is characterized by the presence of PAO, falcate mucro and a few chaetae on the trochanteral organ. This subfamily is composed of only three genera: Capbrya Barra, 1999 from South Africa, Hispanobrya Jordana & Baquero, 2005 from Spain and Nothobrya Arlé, 1961 from Brazil. Nothobrya (type species N. schubarti , described from the state of Pernambuco) remained monospecific for about half a century, when samples taken from urban areas of Rio de Janeiro city revealed its first record for the Brazilian Southeast. This new species, Nothobrya arlei sp. nov., is described and illustrated based on differences related to trochanteral organ, unguis, tenent hair shape and chateae on tenaculum. In this paper, characteristics of the macrochaetotaxy, sensillar and microsensillar sets and ventral tube chaetotaxy are provided, as well as a table with comparisons of Nothobrya species.

KEY WORDS:
Biodiversity; Nothobryinae; restinga; taxonomy

Entomobryidae is very diverse and is distributed worldwide. It was recently revised by Zhang & Deharveng (2014), who integrated molecular data with information on the specialized tergal chaetae. The new classification proposed included seven subfamilies, one of which, Nothobryinae, is characterized by the presence of PAO, falcate mucro and few chaetae on the trochanteral organ.

Nothobrya, one of the three genera of Nothobryinae, was proposed by Arlé (1961) for N. schubarti based on samples collected in the state of Pernambuco, Brazilian Northeast. Samples of N. schubarti had been previously collected by Otto Schubart in the state of Piauí (also Northeast), about 700 km from the type locality. A second genus of Nothobryinae, Capbrya , from South Africa, was described by Barra (1999), who noted its similarity with Nothobrya based on the presence of the PAO, falcate mucro, body segmentation and the absence of scales. Baquero et al. (2005) erected the third Nothobryinae genus, Hispanobrya , with the type species H. barrancoi from Spain. This genus, also monospecific, is similar to Capbrya and Nothobrya by the presence of PAO, absence of scales and falcate mucro. Although Nothobrya shares characteristics with Capbrya and Hispanobrya , it deviates from both genera, especially in the segmentation of the antenna (with six segments).

Nothobrya has remained monospecific until now. However, field work in the vicinity of urban areas of Rio de Janeiro city has revealed the presence of the genus in the Brazilian Southeast. The study of the external morphology from southeastern material has revealed that it consists of a new species, which is herein described.

MATERIAL AND METHODS

The specimens studied were collected using an entomological aspirator at an urban area. The fauna from litter and soil were extracted using Berlese-Tullgren funnels, sorted under a stereomicroscope and mounted on glass slides according to Arlé & Mendonça (1982). Illustrations were made using an optical microscope. The type material was deposited in the Collembola Collection of the Entomology Department, Museu Nacional/UFRJ, Rio de Janeiro, RJ, Brazil (acronym CM/MNRJ).

Abbreviations: (Abd) abdominal segment, (Ant) antennal segment, (MN/UFRJ) Museu Nacional da Universidade Federal do Rio de Janeiro, (PAO) postantennal organ, (Th) thoracic segment.

TAXONOMY

Entomobryidae Schött, 1981

Nothobryinae Zhang & Deharveng, 2014

Nothobrya Arlé, 1961

Nothobrya arlei sp.nov.

Figs. 1-23

urn:lsid:zoobank.org:act:BB1D1965-BEFB-482A-87C0-7D878BEBCED4

Description. Body length up to 2.12 mm. Habitus like Isotomurus . Ground color greenish to pale, with bluish pigment distributed on interocular area and posterior portion of head, distal parts of antennal segments, anterior edges of tergites, and tibiotarsus.

Head. Antennae longer than head; ratio head:antennae = 1.0:1.15. Antennae with six segments, subsegments of first and second antennal segments very small. Ratio of antennal segments: I:II:III:IV:V:VI = 1.0: 3.3: 1.6: 9.3: 5.3: 7.0. Ant.VI with subapical pin seta and about 35 thin sensilla, distributed among ciliated chaetae; apical bulb absent (105 µm) (Fig. 1). Ant. V with two exposed rod-like chaetae, three small proximal sensilla, two guard chaetae and 11 sensilla arranged along the segment (80 µm) (Fig. 2). Ant. IV, the longest segment (140 µm), with about 20 sensilla of different size and thickness; Ant. III with four basal microchaetae, two lateral, one dorsal and one ventral (25 µm) (Fig. 3). Ant. II with only ciliated chaetae (50 µm); Ant. I with one linear series of ciliated chaetae and two smooth microchaetae (15 µm) (Fig. 4). Eyes 8+8, G and H lightly smaller (10 µm). PAO oval with protruding edges (15 µm) (Fig. 5). Labrum with two ciliated chateae, distant from each other, 4/554 smooth labral chaetae and four hook-like papilla on tip (94 µm) (Fig. 6). Maxillary palp simple, with basal chaetae and four sublobal hairs (40 µm) (Fig. 7). Labial palps complete, with five papillae and lateral process not reaching papilla E. Papilla A without chaetae; papilla B with five chaetae (b1, b2, b3, b4 and b5); papilla C without chaetae; papilla D with four chaetae (d1, d2, d3 and d4) and papilla E with four chaetae (e3, e4, e5 and e6); three hipostomal chaetae and five proximal chaetae (Fig. 8).

Figures 1-8
Nothobrya arlei sp. nov. (1) Ant. VI; (2) Ant. V; (3) Ant. IV-III; (4) Ant. II-I; (5) eyepatch with PAO; (6) labrum; (7) maxillary palp and sublobal hairs; (8) labial palps. Scale bars = 20 µm.

Appendages. Trochanteral organ with about 15 lateral smooth spiny chaetae and approximately 40 ciliated chaetae along segment (90 µm) (Fig. 9). Femora with three internal robust macrochaetae measuring 50 µm each (Fig. 10). Tibiotarsi with one robust macrochaeta measuring 60 µm, covered with numerous ciliated chaetae, one on proximal region and six spiny ciliated chaetae on internal region (200 µm) (Fig. 11). Tenent hair pointed. Pretarsi with two short blunt chaetae. Claw elongate, with two basal teeth and one tooth on internal edges, two lateral teeth and one dorsal tooth (65 µm) (Figs. 12, 13). Unguiculi lanceolate, without tooth (30 µm), ratio unguis: unguiculi = 1.0:0.8. Ventral tube with 21 posterior ciliated chaetae, 33 anterior ciliated chateae and 24 apical ciliated chaetae, 2+2 longer than others (126 µm) (Figs. 14, 15). Tenaculum with 4+4 teeth and four long ciliated chaetae (80 µm) (Fig. 16). Dens long, crenulated, with final portion narrowed and striated. Mucro falcate, without basal spine (10 µm) (Fig. 17). Genital plate of male with 20 smooth and subequal chaetae, and 4+4 small eugenital chaetae (36 µm) (Fig. 18).

Figures 9-18
Nothobrya arlei sp. nov. (9) trochanteral organ; (10) femoral and tibiotarsal macrochaetae; (11) tibiotarsus of leg II; (12) unguis; (13) unguis with detail of two lateral and one dorsal teeth; (14) posterior side of ventral tube; (15) anterior side of ventral tube; (16) tenaculum; (17) distal region of dens and mucro; (18) male plate. Scale bars = 10 µm.

Body chaetotaxy: Body densely covered by chaetae of several sizes (Fig. 19), bothriotrica and sensilla. Head with macrochaetae on interocular area, lateral and posterior edges. Body with macrochaetae type two on thoracic and abdominal tergites (Figs. 20, 21); Th. II, III and Abd. I with several asymmetries, especially on distal portions on tergites. Bothriotricha on abdominal tergites II/III/IV: 2/3/2. Sensillary chaetotaxy of Th. II - Abd. V: Microsensilla: 1,0/1,0,0,0,0 (Figs. 22, 23); Sensilla: 1,2/1,3,3,8,3. Pseudopores not clearly visualized in tergites.

Figures 19-23
Nothobrya arlei sp. nov. (19) types of chaetae present on body; (20) body macrochaetotaxy of Th. II-III and Abd. I-V; (21) detail of Abd. IV; (22) detail of Th. II; (23) detail of Abd. I. Scale bars = 10 µm (19, 21-23), 100 µm (20).

Type material. Holotype male on slide number 1937a CM/MNRJ Recreio dos Bandeirantes, Rio de Janeiro, 15/III/2009, Silveira, T.C. col. Locality: urban area previously covered by native "restinga" vegetation, sand beach and a large lacunar lagoon system, 22°59'51.10"S, 43°25'14.45"W, about 3 m a.s.l.Nine paratypes: slides numbers 1937a CM/MNRJ, 1937b CM/MNRJ, 1937c CM/MNRJ, 1937d CM/MNRJ, 1937e CM/MNRJ, 1937f CM/MNRJ, 1937g CM/MNRJ, 1937h CM/MNRJ, 1937i CM/MNRJ, same data as holotype. Ten paratypes in slides numbers 1940a CM/MNRJ, 1940b CM/MNRJ, 1940c CM/MNRJ, 1940d CM/MNRJ, 1940e CM/MNRJ, 1940f CM/MNRJ, 1940g CM/MNRJ, 1940h CM/MNRJ, 1940i CM/MNRJ, 1940j CM/MNRJ, 27/III/2009. Two paratypes in ethanol, number 1940. Silveira, T.C; Mendonça, M.C.; Fernandes, L.H & Bernardo, A.L. col., same locality as holotype.

Etymology. The species epithet is in honor of Roger Arlé, the author of Nothobrya .

Remarks. The presence of Nothobrya in "restinga" areas configures its first record from the Southeast, distant about 1,700 km from the type locality of the genus. Both areas, despite the distance, are characterized by high temperature and sand soil.

The description of N. schubarti by Arlé (1961) is brief and lacks details of the morphology and general chaetotaxy, preventing an adequate comparison between it and the new species. Additionally, study of paratypes deposited in the Collembola Collection of the National Museum/UFRJ has not allowed the visualization of several characters due to the precarious condition of this material. However, the redescription of Baquero et al. (2004), based on topotypical material of N. schubarti , shows differences related to the trochanteral organ, number of teeth on unguis, shape of tenent hair, and chaetae on tenaculum (Table 1).

Table 1
Comparisons of Nothobrya Arlé, 1961 species.

Characteristic	N. schubarti Arlé, 1961	N. arlei sp. nov.
Body size	0.95-2 mm	0.72-2.12 mm
Body pigment	greenish with blue pigment	greenish to pale with bluish pigment
Labral formula	4/554	4/554
Maxillary palp/Sublobal hairs	?	Simple/4
Labial palp	?	five papillae
Trochanteral organ	3-4 smooth chaetae	about 15 smooth chaetae
Tenent hair	truncated	pointed
Tita spines	?	6
Tenaculum chaetae	2 chaetae	4 ciliated chaetae
Mucro	falcate	falcate
Ventral tube chaetae	?	21 posterior, 33 anterior, 24 apical
Tergal sensillary formula	?	1,2/1,3,3,8,3
Tergal microsensillary formula	?	1,0/1,0,0,0,0
Shape of chaetae	type two and five	type two and five
Botriotricha	2/3/2	2/3/2
Distribution	Pernambuco and Piauí states	Rio de Janeiro state

Nothobrya arlei sp. nov. shares similarities with N. schubarti such as the habitus, color, body size, type of chateae and falcate mucro. Nonetheless, the presence of 15 lateral smooth spiny chaetae with numerous ciliate chaetae on the trochanteral organ differentiates this species, since N. schubarti shows 3-4 chaetae, none of which is spiny. The unguis in N. arlei sp. nov. is also a reliable characteristic for species discrimination: in the new species, it has two teeth on inner margin, two lateral and one dorsal tooth, while in the redescription of N. schubarti there is reference only to the presence of two basal teeth. Comparisons also revealed that N. arlei sp. nov. displays four long ciliated chaetae on the tenaculum, whereas N. schubarti shows only two chateae. Moreover, the legs of N. arlei sp. nov. have three robust macrochaetae on femora, six ciliated spines and one robust macrochaeta on the proximal region of tibiotarsi. In the redescription of Baquero et al. (2004) no observation was made about the leg chaetotaxy of N. schubarti , except for the spatulate shape of the tenent hair, which Arlé (1961) refers to as pointed, a characteristic also observed in N. arlei sp. nov. The general chaetotaxy of both species is similar, with chaetae of type two and five (Christiansen 1958) and the same number of bothriotricha (2-3-2) on Abd. II/III/IV, respectively. In the specimens of N. arlei sp. nov. herein studied, the distribution of the macrochaetae from Th. II - Abd. I shows some asymmetries, but from the Abd. II onward a pattern is noted. Although the macrochaetotaxy and sensillar pattern of N. shubarti is unknown, the differences verified in individuals of N. arlei sp. nov. seem sufficient to support this species as the second of the genus.

ACKNOWLEDGMENTS

We are thankful to Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) for financial support (process E-26/111.504/2013); Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the scholarship to Tatiana Cristina da Silveira; Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPQ) for a grant to Maria Cleide de Mendonça (process 307644/2015-4); and Dr. Eduardo Assis Abrantes for reviewing the manuscript.

LITERATURE CITED

• Arlé R (1961) Novas espécies de colêmbolas aquáticas (Nota preliminar). Atas da Sociedade de Biologia do Rio de Janeiro 5: 34-37.
• Arlé R, Mendonça MC (1982) Estudo preliminar das espécies de Dicranocentrus Schött, 1893, ocorrentes no Parque Nacional da Tijuca, Rio de Janeiro (Collembola). Revista Brasileira de Biologia 42: 41-49.
• Barra J-A (1999) Un nouveau genre Capbrya avec deux nouvelles espèces de la Province du Cap (Rép. Sud Africaine) (Collembola: Entomobryidae), Capbrya n. gen. d'Afrique du Sud (Insecta: Collembola). Bulletin de l'Institute Royal des Sciences Naturelles de Belgique 69: 19-24.
• Baquero E, Jordana R, Christiansen K (2004) Redescription of Nothobrya schubarti Arlé, 1961 (Collembola, Entomobryomorpha). Entomological News 115: 31-34.
• Baquero E, Martinez M, Christiansen K, Jordana R (2005) A new genus and species of Entomobryidae (Collembola, Entomobryomorpha) from the Iberian Peninsula. Entomological News 115: 229-235.
• Christiansen KA (1958) The Nearctic members of the genus Entomobrya (Collembola). Bulletin of the Museum of Comparative Zoology 118: 437-545.
• Zhang F, Deharveng L (2014) Systematic revision of Entomobryidae (Collembola) by integrating molecular and new morphological evidence. Zoologica Scripta 44: 298-311. doi: 10.1111/zsc.12100
  » https://doi.org/10.1111/zsc.12100

• Editorial responsibility:

  Gabriel L.F. Mejdalani

• ZooBank:

  urn:lsid:zoobank.org:pub:4187E372-19BA-446C-BC7D-F4FCBD2C6AA0

Publication Dates

• Publication in this collection
  2016

History

• Received
  06 July 2016
• Reviewed
  01 Sept 2016
• Accepted
  11 Sept 2016