Two new species of Salina MacGillivray (Collembola, Paronellidae) with rectangular mucro from South America

ABSTRACT

Two new species of Salina, S. maculiflora sp. nov. from Brazil and S. colombiana sp. nov. from Colombia are described and illustrated. The complete dorsal chaetotaxy, including the specialized chaetae (S-chaeta), is studied in these new species. Comparisons based on the chaetotaxy of the basomedian field, abdomen II, and mucro shape are made between species from groups beta, celebensis, and borneensis. This is the first record of Salina with rectangular mucro (beta group) in South America and a key to the seven Nearctic and Neotropical species is provided.

Keywords:
Chaetotaxy; Cremastocephalini; Neotropics; Species group; S-chaeta

Introduction

Salina MacGillivray is a genus of paronellids with currently 71 nominal species widely distributed in America, Africa, and south Asia (Bellinger et al., 2015). Salina species resemble other genera of Cremastocephalini (sensu Mitra, 1993), such as Akabosia Kinoshita, 1919, by the absence of scales, dorsal chaetotaxy and dens with one spatulated and enlarged distal appendix (Szeptycki, 1979; Mitra, 1993). However, Salina is distinguished from other genera by the presence of an interocellar macrochaeta and dens not crenulate (Yoshii, 1983; Mitra, 1993; Soto-Adames, 2010).

Based on the shape of the mucro, dental appendage and tergal macrochaetotaxy, Mitra (1973, 1993) proposed two species groups within Salina: celebensis and indica. Posteriorly, Yoshii (1981, 1983) studied the chaetotaxy of the first two abdominal segments and included the groups beta, borneensis and saikehi alongside celebensis, while excluding the indica group.

Soto-Adames (2010) recently reviewed the beta group and proposed a new diagnosis, mainly characterized by the rectangular mucro with two main teeth and the second abdominal segment with one external and one central macrochaeta. So far, the beta group is exclusively found in the New World and contains five species: Salina betaChristiansen and Bellinger, 1980 from the United States, S. ventricolor Gruia, 1983 from Cuba, S. wolcottiFolsom, 1927 from Puerto Rico, and S. bidentata (Handschin, 1927) and S. thibaudiSoto-Adames, 2010 from Costa Rica. None of them is recorded from South America (Soto-Adames, 2010; Bellinger et al., 2015).

Herein, we describe two new species of Salina with rectangular mucro from South America, providing detailed information on dorsal chaetotaxy and an identification key for Salina beta species group.

Material and methods

Specimens were preserved in 80% ethanol, clarified with potassium dichromate (K₂Cr₂O₇) and hydrochloric acid (HCl) and mounted on glass slides with Hoyer liquid. We followed the procedures described by Arlé and Mendonça (1982) and Christiansen and Bellinger (1998), respectively. Specimens were photographed in ethanol gel using a stereomicroscope (M165C) attached to a DFC420 digital camera. Photographs were digitally corrected using Leica Application Suite V3.4.1. Type material is deposited at the Invertebrate Collection of Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, Brazil, and "Instituto de Ciencias Naturales" (ICN/UNAL), Universidad Nacional de Colombia, Bogotá, Colombia.

The system used in the descriptions of the species follows Soto-Adames (2010), except Mitra and Dallai (1980) for mucro description. The labial chaetotaxy follows Fjellberg (1999). Nomenclature of the head dorsal chaetotaxy follows the AMS system of genera Entomobrya, Rondani 1861, Seira Lubbock, 1870 and Trogolaphysa Mills, 1938 (Jordana and Baquero, 2005; Soto-Adames, 2008; Soto-Adames and Taylor, 2013), body follows Szeptycki (1979) based on the genus Akabosia, and tergal specialized chaetae (S-chaeta) of Entomobryidae according to Zhang and Deharveng (2015). Chaetae of uncertain homology are followed by a question mark (?). Abbreviations used in the text: Abd. = abdominal segment, Ant. = antennal segment, Th. = thoracic segment, mac. = macrochaeta(e), mes. = mesochaeta(e), mic. = microchaeta(e), sens. = sensilla(e).

Results

Salina maculiflora sp. nov.

See Figs. 1–27.

Fig. 1
Salina maculiflorasp. nov.: habitus of a specimen in ethanol (Ant. III and IV missing).

Figs. 2–8
Salina maculiflora sp. nov.: (2) symbols used in detailed chaetotaxy schemes; (3) head dorsal chaetotaxy; (4) apical bulb of Ant. IV (dorsal view); (5) Ant. I dorsal chaetotaxy (right); (6) Ant. I ventral chaetotaxy; (7) prelabral chaetae; (8) labral chaetotaxy.

Figs. 9–20
Salina maculiflora sp. nov.: (9) labial palp; (10) maxillary outer lobe; (11) right and left mandibles (right molar plate omitted); (12) basomedian and basolateral field of labium; (13) head ventral chaetotaxy; trunk dorsal chaetotaxy: (14) Th. II, (15) Th. III, (16) Abd. I, (17) Abd. II, (18) Abd. III, (19) Abd. IV, (20) Abd. V.

Figs. 21–27
Salina maculiflora sp. nov.: (21) trochanteral organ; (22) distal tibiotarsus and foot I complex; (23) distal tibiotarsus and foot III complex; (24) collophore anterior side; (25) posterior and lateral side of collophore; (26) distal dens and mucro with two teeth; (27) distal dens and mucro with three teeth. 22-23, arrows indicate the monocondyle of the tibiotarsus.

Diagnosis. Distinguished by flower-shaped blue spots on Th. III to Abd. IV; dorsal head with chaeta A5; Ant. I dorsally with 4 mac.; basomedian field with two ciliated chaetae (M2 and E); Th. II to Abd. II respectively with 1 (p2), 4 (p1-3, p5), 2 (m3-4) and 3 (m3, m3e, m5) central mac. per side; Abd. IV without A4 mac.; collophore anterior side with 8 + 8 chaetae and posterior side with 3 + 3 chaetae (Figs. 1, 3, 5, 12, 14–17, 19, 24, 25).

Description. Total length of the holotype 1.7 mm. Habitus typical of paronellids of Cremastocephalini tribe (sensu Mitra, 1993) (Fig. 1). Specimens predominantly pale to light yellow aspect, with blue pigment covering the distal region of Ant. II-III, Ant. I base, anterior and lateral sides of head; lateral of Th. II to Abd. V; Th. III with 3 + 3 rosette-like blue spots, Abd. I, II and IV with 2 + 2, 4 + 4 and 6 + 6 flower-shaped spots, respectively; Abd. III and. IV with blue spots posteriorly. Femur I-III with one and tibiotarsi I-III with two light blue spots distally; eyepatch area black (Fig. 1).

Head. Eyepatches oval, with largest ocelli A and B and smallest G and H, with three interocular ciliated chaetae (Fig. 3). Head dorsal chaetotaxy as in Fig. 3; antennal series 'An' with 6 + 6 chaetae, An1a, An1, An2, An3a and An3 as mac., An2a as spine-like mic.; anterior series 'A' with A5 mes.; medio-ocellar series 'M' with 3 + 3 chaetae, M4 as mac., M0 and M2 as mes.; sutural series 'S' with 3 + 3 chaetae, S2 and S3 as mac., S7 as mes.; interocular series with 3 + 3 chaetae, r as mac., p and t as mic.; postoccipital anterior series 'Pa' with 3 + 3 chaetae, Pa5 and one typical chaeta (P5a) as mac., Pa6 as bothriotricum; postoccipital median series 'Pm' with 2 + 2 mac. (Pm1 and Pm3); postoccipital posterior series 'Pp' with 1 + 1 mac. (Pp1); postoccipital external series 'Pe' with mac. Pe3 present. Ant. IV with a simple apical bulb and smooth and ciliated chaetae. Ant. I with 4 + 4 dorsal mac.; dorsal base with 5 + 5 to 6 + 6 sensillae-like smooth mic. and ventral base with 12 + 12 (Figs. 5 and 6). Four prelabral ciliated chaetae and 14 labral smooth chaetae (4/5/5), four anterior (a1-2), a1 spine-like; five median (m0-2), and five posterior (p0-2) (Figs. 7 and 8). Labial palp with five smooth proximal chaetae and six papillae (A-E and H), A and C simple, H with two smooth guard appendages (h1-2), B with five (a1, b1-4), D with three (d1-2 and d4), and E with lateral process (l.p.) smaller than the papilla and two smooth guard appendages (e1-2) (Fig. 9). Maxillary outer lobe with apical appendage (a.a.) and basal chaeta (b.c.) of same length, both smooth, sublobal plate with three internal smooth appendages (Fig. 10). Right mandible (ventral view) with four incisive teeth, left mandible with five teeth; both mandibles with six stronger molar teeth (Fig. 11). Basolateral and basomedian field with chaetae A1-5 smooth (A5 thickest), M2, E, L1 and L2 ciliated, r and M1 absent (Fig. 12). Cephalic groove (CG) with 8 + 8 chaetae, 5 + 5 ciliated (CG1-3, CG5 and CG7), 1 + 1 smooth (CG8), and 2 + 2 as spine-like mic. (CG4 and CG6); medial postlabial (PLM) with 1 + 1 ciliated chaetae (PLM1); external postlabial (PLE) with 4 + 4 ciliated chaetae (PLE1-4). Head ventral chaetotaxy as in Fig. 13.

Thorax dorsal chaetotaxy. Th. II as in Fig. 14; anterior series 'a' with 10 + 10 unnamed mac. of anterior collar, one S-microchaeta (ms), and one anterolateral sens. (al); medial series 'm' with 3 + 3 chaetae, m7 as mac., m1 and m2 as mes. present or absent, plus 1 + 1 unnamed mac. laterally; posterior series 'p' with 2 + 2 chaetae, p2 as mac., p1 as mes. present or absent. Th. III dorsal chaetotaxy as in Fig. 15; series 'p' with 6 + 6 mac. (p1-3, p5 and 2 + 2 unnamed chaetae), and one anterolateral sens. (al).

Abdomen dorsal chaetotaxy. Abd. I as in Fig. 16; series 'm' with 3 + 3 chaetae, m3 and m4 as mac., m5 as mes., and one S-microchaeta (ms). Abd. II as Fig. 17; series 'a' with a5 as bothriotricum; series 'm' with 4 + 4 chaetae, m3, m3e and m5 as mac., m2 as bothriotricum; series 'p' with 2 + 2 chaetae, p6 as mac. present or absent, p7 as mes. plus el mac. Abd. III as in Fig. 18; series 'a' with 3 + 3 chaetae, a5 as bothriotricum, a7 and am6 as mes.; series 'm' with 2 + 2 bothriotricha (m2 and m5); series 'p' with 3 + 3 chaetae, p6 and pm6 as mac., p7i as mes. One anterosubmedial sens. (as) present. Abd. IV as in Fig. 19; series 'A' with 3 + 3 chaetae, A1 and A6 as mac., A3 as mes.; series 'Ae' with Ae1 as mac.; series 'B' with 4 + 4 chaetae, B3-5 as mac., B6 as bothriotricum; series 'Be' with Be1 as mac.; series 'C' with C1 as mac.; series 'T' with 2 + 2 bothriotricha (T2 and T4), and one S-microchaeta (ms); series 'E' with 2 + 2 mac. (E1-2); series 'F' with 4 + 4 mac. (F1-3p); series 'Fe' with 5 + 5 chaetae, Fe1-3 as mac., Fe4-5 as bothriotricha; posterior margin with 5 + 5 unnamed ciliated mes., and three sens. presents (ps and two unnamed). Abd. V as in Fig. 20; series 'a' with 3 + 3 chaetae, a5 as mac., a3 and a6 as mes.; series 'm' with 4 + 4 or 5 + 5 mac. (m2-5e), m5a present or absent; series 'p' with 5 + 5 or 6 + 6 chaetae, p1, p3-5 and ap6 (present or absent) as mac., pp6 as mes.; one anterosubmedial sens. (as) and two accessory sens. (acc.p4 and acc.p5) present.

Tergal S-chaetae formula 1, 0| 1, 0, 0, 1, 0 (ms) and 1, 1| 0, 0, 1, 3, 3 (sens) of Th. II to Abd. V (Fig. 14–20).

Legs. Trochanteral organ with 14 spine-like chaetae (Fig. 21). Unguis I-II (same morphology) with three unpaired inner teeth, a basal, a median and one at the apex (Fig. 22). Unguis III with one unpaired inner tooth near the apex (Fig. 23). Unguiculi trilamelate, lamellae inner truncate, lamellae external acuminate, both smooth edges. Tenent hairs capitate, weakly ciliated, present on pretarsus. All tibiotarsi with one socket monocondyle at the apex (Figs. 22 and 23). Tibiotarsus III with a smooth distal chaeta, near unguiculus base (Fig. 23).

Collophore. Anterior side with 3 + 3 long ciliated mac. and 5 + 5 smooth mic.; posterior side with 2 + 2 smooth mic. and 1 + 1 ciliated; lateral side with 14 + 14 smooth mic. (Figs. 24 and 25).

Furcula. Dens with rows of ciliated chaetae and mucro with two main teeth (d1 and v1) and one reduced accessory teeth present or absent (ap) (1 out of 14 specimens) (Figs. 26 and 27).

Type material. Holotype female, on slide N° COLLE 040/INPA: Brazil, Amazonas, Rio Preto da Eva municipality, "Aprisco Pásargada" farm (02°42'26.6"S; 59°42'53.2"W), Amazon forest, 13.ix.2013, 45 m, Malaise trap, BG Oliveira coll. Paratypes on slide N° COLLE 040A-G/INPA: 3 males, 7 females in slides, and 4 specimens in ethanol, same data as holotype. 3 paratypes in ethanol, same data as holotype, except date: 13.xii.2013.

Other examined material. 1 immature on slide, Brazil, Amazonas, Presidente Figueiredo municipality, AM-270, Km 18 (02°02'48"S; 59°52'01"W), 30.viii.2014, 146 m, dish trap, NG Cipola and FGL Oliveira coll. 2 females on same slide, Manaus municipality, "Raifran" farm, entrance to "Brasileirinho" Km 7 (03°02'08"S; 59°52'16"W), 29.viii.2013, 38 m, BG-Malaria trap, LB Leal coll. 1 female on slide, Novo Airão municipality, "Mato Grosso" stream (02º49'00"S; 60°55'08"W), 28-31.iii.2013, dish trap, JT Câmara and AC Maldaner coll. All deposited in INPA.

Etymology. Refers to its distinct color pattern resembling flowers (from Latin: macula = spot and flos = flower) (Fig. 1).

Distribution and habitat. This species was found only in the Amazon forest, Amazonas State, Brazil and in Good's biogeographic zone 26 of Neotropical region, Highlands of Eastern Brazil: North Brazilian (Good, 1974). The climate of the area is equatorial monsoonal (Am) (Kottek et al., 2006). This is the first species of Salina with rectangular mucro described from South America, and the first species of Salina described from Brazil.

Salina colombiana sp. nov.

See Figs. 28–41.

Fig. 28
Salina colombianasp. nov.: habitus of a specimen in ethanol.

Figs. 29–41
Salina colombiana sp. nov.: (29) head dorsal chaetotaxy; (30) Ant. I dorsal chaetotaxy (left); (31) basomedian and basolateral field of labium; (32) head ventral chaetotaxy; trunk dorsal chaetotaxy: (33) Th. II, (34) Th. III, (35) Abd. I, (36) Abd. II, (37) Abd. IV, (38) Abd. V; (39) trochanteral organ; (40) collophore anterior side; (41) posterior and lateral side of collophore.

Diagnosis. Distinguished by strong yellow color on body; dorsal head with S6 mes. and without chaetae An1a and M0; Ant. I dorsally with 7 mac.; basomedian field with two ciliated chaetae (M2 and E); Th. II to Abd. II respectively with 7 (a5, m1-2, m4, p1-3), 6 (p1-5), 3-4 (m3-4) and 3 (m3, m3e, m5,) central mac. per side; Abd. IV with A3 and A4 mac.; collophore anterior side with 10 + 10 chaetae and posterior side with 5 + 5 chaetae (Figs. 28–31, 33–37, 40, 41).

Description. Total length of the holotype 2.25 mm. Habitus typically of paronellids of Cremastocephalini tribe (sensu Mitra, 1993) (Fig. 28). Specimens with strong yellow color covering the whole body; eyepatch area black (Fig. 28).

Head. Eyepatch oval, with largest ocelli A and B and smallest G and H, with three interocular ciliated chaetae (Fig. 29). Head dorsal chaetotaxy as in Fig. 29; antennal series 'An' with 5 + 5 chaetae, An1, An2, An3a and An3 as mac., An2a as spine-like mic.; anterior series 'A' with A5 mes.; medio-ocellar series 'M' with 2 + 2 chaetae, M2 as mes. and M4 as mac.; sutural series 'S' with 4 + 4 chaetae, S2 and S3 as mac., S6 and S7 as mes.; interocular series with 3 + 3 chaetae, r as mac., p and t as mes.; postoccipital anterior series 'Pa' with 3 + 3 or 4 + 4 chaetae, Pa2?, Pa5 and one typical chaeta (P5a) as mac., Pa6 as bothriotricum; postoccipital median series 'Pm' with 2 + 2 mac. (Pm1 and Pm3); postoccipital posterior series 'Pp' with 1 + 1 mac. (Pp1); postoccipital external series 'Pe' with mac. Pe3 present. Ant. IV with a simple apical bulb and smooth and ciliated chaetae (similar to S. maculiflora sp. nov., Fig. 4). Ant. I with 7 + 7 dorsal mac. and dorsal base with 6 + 6 sensillae-like smooth mic. (Fig. 30); Four prelabral ciliated chaetae and 14 labral smooth chaetae (4/5/5), four anterior (a1-2), a1 spine-like; five median (m0-2), and five posterior (p0-2) (similar to S. maculiflora sp. nov., Figs. 7 and 8). Labial palp with five smooth proximal chaetae and six papillae (A-E and H), A and C simple, H with two smooth guard appendages (h1-2), B with five (a1, b1-4), D with three (d1-2 and d4), and E with lateral process (l.p.) smaller than the papilla and two smooth guard appendages (e1-2) (similar to S. maculiflora sp. nov., Fig. 9). Maxillary outer lobe with apical appendage (a.a.) and basal chaeta (b.c.) of same length, both smooth, sublobal plate with three internal smooth appendages (similar to S. maculiflora sp. nov., Fig. 10). Right mandible (ventral view) with four incisive teeth, left mandible with five teeth; both mandible with six molar teeth (Fig. 11). Basolateral and basomedian field with chaetae A1-5 smooth (A5 thickest), M2, E, L1 and L2 ciliated, r and M1 absent (Fig. 31). Cephalic groove (CG) with 9 + 9 or 10 + 10 chaetae, 7 + 7 ciliated (CG1-3, CG5, CG8-10), CG10 as ciliated or spine-like mic., CG4, CG6 and CG7 (present or absent) as spine-like mic.; medial postlabial (PLM) with 2 + 2 ciliated chaetae (PLM1-2); external postlabial (PLE) with 2 + 2 ciliated chaetae (PLE1-2). Head ventral chaetotaxy as in Fig. 32.

Thorax dorsal chaetotaxy. Th. II as in Fig. 33; series 'a' with 11 + 11unnamed chaetae of anterior collar, a5 mac. present; S-microchaeta (ms), and one anterolateral sens. (al); medial series 'm' with 4 + 4 mac. (m1, m2, m4 and m7) and 3 + 3 unnamed chaetae laterally; posterior series 'p' with 3 + 3 mac. (p1-3). Th. III as in Fig. 34; series 'p' with 7 + 7 mac. (p1-5 and one unnamed); one anterolateral sens. (al), and three unnamed mes.

Abdomen dorsal chaetotaxy. Abd. I as in Fig. 35; series 'm' with 4 + 4 or 5 + 5 mac. (m2-5 and one unnamed), m2 present or absent, and one S-microchaeta (ms). Abd. II as Fig. 36; series 'a' with a5 as bothriotricum; series 'm' with 4 + 4 chaetae, m3, m3e and m5 as mac., m2 as bothriotricum; series 'p' with 2 + 2 chaetae, p6 as mac., p7 as mes.; chaeta el absent. Abd. III as in Fig. 18 (the same to S. maculiflora sp. nov.); series 'a' with 3 + 3 chaetae, a5 as bothriotricum, a7 and am6 as mes.; series 'm' with 2 + 2 bothriotricha (m2 and m5); series 'p' with 3 + 3 chaetae, p6 and pm6 as mac., p7i as mes. One anterosubmedial sens. (as) present. Abd. IV as in Fig. 37; series 'A' with 4 + 4 mac. (A1, A3, A4 and A6); series 'Ae' with Ae1 as mac.; series 'B' with 4 + 4 chaetae, B3-5 as mac., B6 as bothriotricum; series 'Be' with Be1 as mac.; series 'C' with C1 as mac.; series 'T' with 2 + 2 bothriotricha (T2 and T4), and one S-microchaeta (ms); series 'E' with 3 + 3 mac. (E1-2 and E4); series 'F' with 4 + 4 chaeta, F1-3 as mac., F3p as mes.; series 'Fe' with 4 + 4 chaetae, Fe1 and Fe3 as mac., Fe4 and Fe5 as bothriotricha; median region with one unnamed mes.; posterior margin with 3 + 3 to 5 + 5 unnamed mes., and four sens. present (ps and three unnamed). Abd. V as in Fig. 38; series 'a' with 2 + 2 or 3 + 3 chaetae, a5-6 as mac., a3 as mac. or mic. present or absent; series 'm' with 3 + 3 mac. (m2-3 and m5); series 'p' with 5 + 5 mac. (p1, p3-5 and ap6); one anterosubmedial sens. (as) and two accessory sens. (acc.p4 and acc.p5) present.

Tergal S-chaetae formula 1, 0| 1, 0, 0, 1, 0 (ms) and 1, 1| 0, 0, 1, 4, 3 (sens) of Th. II to Abd. V (Figs. 33–38).

Legs. Trochanteral organ with 18 spine-like chaetae (Fig. 39). Unguis I-II (same morphology) with three unpaired inner teeth, a basal, a median and one at the apex (similar to S. maculiflora sp. nov., Fig. 22). Unguis III with one unpaired inner teeth near the apex (similar to S. maculiflora sp. nov., Fig. 23). Unguiculi trilamelate, lamellae inner truncate, lamellae external acuminate, both smooth edges. Tenent hairs capitate, weakly ciliated, present on pseudotarsus. All tibiotarsi with one socket monocondyle at the apex of tibiotarsus (Figs. 22 and 23). Tibiotarsus III with a smooth distal chaeta, near unguiculus base (Fig. 23).

Collophore. Anterior side with 3 + 3 long ciliated mac., 1 + 1 ciliated mes. and 6 + 6 smooth mic.; posterior side with 4 + 4 smooth mic. and 1 + 1 ciliated; lateral side with 13 + 13 smooth mic. (Figs. 40 and 41).

Furcula. Dens with rows of ciliated chaetae and mucro two teeth, d1 and v1 (4 out of 5 specimens) and sometimes with one reduced accessory teeth present (ap) (1 out of 5 specimens) (Figs. 26 and 27).

Type material. Holotype female, on slide deposited in ICN/UNAL: Colombia, Nariño, San Andres de Tumaco municipality, University campus (01°48'N; 78°452'W), Andean Region, 4-14.iii.2015, 3 m, Malaise trap, Animal Taxonomy students coll. Paratypes on slides deposited in ICN/UNAL: 1 male, 2 females and in alcohol 31 specimens in ethanol, same data as holotype. Paratypes on slide N° COLLE 041A-C/INPA: 3 females and in 10 specimens in ethanol, same data as holotype.

Other examined material. 1 female and 1 immature on slide, Colombia, Guaviare Department, San José del Guaviare municipality (02°34'06"N; 72°41'36"W), 18.iv.2013, 192 m, Malaise trap, Animal Taxonomy students coll. 1 male and 1 female on slide and 7 specimens in ethanol, Playa Guio, 14.iv.2013. All deposited in ICN/UNAL.

Etymology. Refers to its type locality, in Colombia.

Distribution and habitat. This species was found in areas of Amazon forest, Guaviare Department and low Andes Region, Tumaco municipality, both in equatorial area of Colombia. These locations are situated respectively in Good's biogeographic zone 26 and 28 of Neotropical region (Good, 1974). The climate of the area is "Af" tropical rain florest climate, characterized by high humidity (Kottek et al., 2006). The new species represents the first record of Salina with rectangular mucro from Colombia.

Discussion

Recently, Zhang et al. (2015) proposed a great change in Entomobryoidea taxonomy by supporting tergal specialized chaetae (S-chaeta) as the strongest morphological character for separating genera, what led to many classification changes within its families and subfamilies. Salina is also included in this context and its S-chaetae pattern of Th. II to Abd. V= 1, 1| 0, 0, 1, 3 (sens) (excluding Abd. IV, see Zhang et al. 2015), was corroborated in S. maculiflora sp. nov. and S. colombiana sp. nov. This character and other features, such as the S-microchaetae pattern of Th. II to Abd. V= 1, 0| 1, 0, 0, 1, 0 (ms), revealed here for the first time in Salina, have often been omitted in many species descriptions (Mitra, 1973, 1993; Yoshii, 1981, 1983; Soto-Adames, 2010). Therefore, we argue they should be further investigated in the genus, as they have been useful to separate other Entomobryoidea (Jantarit et al., 2013; Zhang and Deharveng, 2015).

In this sense, the species groups of Salina recently proposed by Soto-Adames (2010), must also be further phylogenetically analyzed, especially in a phylogenetic context, because morphological characteristics used in their diagnoses are unstable (Table 1). For example, in the beta group (species with rectangular mucro), the basomedian field has only smooth chaetae, but the two new species, which also present rectangular mucro, S. maculiflora sp. nov. and S. colombiana sp. nov. have two ciliated chaetae (M2 and E) (typical celebensis group sensu Yoshii, 1981, 1983).

Table 1
Comparison of morphological characters among selected species of Salina and their species groups.

Species	Species group	Ant. I DM	Th. II CM	Th. III CM	Abd. I CM	Abd. II CM	Collophore posterior chaetae	Unguiculus shape	Mucro shape/No of teeth
S. maculiflora sp. nov.	beta	4	1	4	2	2, 1 [m3, m3e, m5]	3 + 3	Truncate	Rectangular
BR									2-3 teeth
S. colombiana sp. nov.	beta	7	7	6	3 (4)	2, 1 [m3, m3e, m5]	5 + 5	Truncate	Rectangular
CO									2-3 teeth
S. fasciata b	beta?	?	5	8	6	2, 2 [m3, m3e, m5, a6?]	?	Truncate	Rectangular
ID									3 teeth
S. beta e	beta	2	4	5	4	1, 1 [m3, m5]	1	Truncate	Rectangular
USA									3 teeth
S. thibaudi e	beta	4	7 (8)	6 (5-9)	4 (3-6)	1, 1 [m3, m5]	3 + 3 (3-6)	Truncate	Rectangular
CR									2-3 teeth
S. wolcotti e	beta	2-3	3 (3-5)	4 (2-4)	2 (2-3)	1, 1 [m3, m5]	1 + 1	Truncate	Rectangular
PR									2-3 teeth
S. celebensis a , e	celebensis	?	1	2	2	2, 1 [m3, m3e, m5]	8 + 8	Truncate	Square 3
CR, PR									teeth
S. dedoris c , e	celebensis	4	6	8	3	2, 1 [m3, m3e, m5]	2 + 2 (0-2)	Truncate	Square 3-4
CO									teeth
S. mulcahyae d , e	borneensis	?	?	?	13	2, 2 [m3, m3e, m5, a6?]	?	Lanceolate	Square 3
USA									teeth
S. saikehi b	borneensis	?	0	2	4	2, 2 [m3, m3e, m5, a6?]	9 + 9	Truncate	Square 3
ID									teeth

• Abbreviations and symbols used to represent the morphological characteristics: DM, dorsal mac.; CM, central mac.; BR, Brazil; CO, Colombia; CR, Costa Rica; ID, Indonesia; PAN, Panama; PR, Puerto Rico; USA, United States;?, unknown; (), chaetal variation; [], chaetal nomenclature.
• ^a
  Yoshii (1981).
• ^b
  Yoshii (1983).
• ^c
  Mari-Mutt (1987).
• ^d
  Christiansen and Bellinger (1998).
• ^e
  Soto-Adames (2010).

Another example is seen on Abd. II dorsal chaetotaxy, which was first proposed by Mitra (1973), modified and Yoshii (1981, 1983) and partly followed by Soto-Adames (2010) for the separation of Salina groups, was based on the following central mac. formulas: 1,1 (m3 and m5); 2,1 (m3, m3e and m5) and 2,2 (m3, m3e, m5, a6?) for beta, celebensis and borneensis group, respectively (the last two have a square mucro). In S. maculiflora sp. nov. and S. colombiana sp. nov. the Abd. II has 2,1 central mac. (typical of celebensis group), while in S. fasciata (Handschin, 1928), from Indonesia, and with a rectangular mucro (after Yoshii, 1983: 23) the Abd. II has 2,2 central mac. (typical of borneensis group) (Table 1).

Thus, it is clear that the separation of species groups based on the presence or absence of two chaetae (a6?, m3e) on Abd. II is insufficient, since the remaining characteristics, such as basomedian field chaetae type, are variable within groups. Therefore, for instance, the only character able to separate Salina species groups may be the mucro: rectangular mucro with two main teeth (d1 and v1) and one reduced or absent accessory tooth (ap) (beta group), or square mucro with three main teeth (d1, ap and v1) and a reduced or absent basal tooth (v2) (celebensis group).

Within the beta group and apart from Abd. II mac. formula, S. maculiflora sp. nov. resembles S. wolcottiFolsom, 1927 (see Soto-Adames, 2010) in the color pattern with flower-shaped spots, collophore anterior side with 3 + 3 long ciliated mac., dorsal chaetotaxy of Th. III, and Abd. I respectively with 4 + 4 and 2 + 2 central mac. (Table 1). However, S. maculiflora sp. nov. differs from this species by Ant. I dorsally with 4 mac. (3 in S. wolcotti) and 6 sensillae-like smooth mic. (4 in S. wolcotti), four prelabral chaetae (two in S. wolcotti), and collophore posterior side with 3 + 3 smooth chaetae (1 + 1 in S. wolcotti) (Table 1). In addition, S. maculiflora sp. nov. also differs in Th. II dorsal chaetotaxy with 1 + 1 (p2) central mac. (5 + 5 in S. wolcotti), and Th. III with 1 + 1 extranumerary mac. anterolaterally (none in S. wolcotti).

Salina colombiana sp. nov. resembles S. thibaudiSoto-Adames, 2010 by the chaetotaxy pattern of Th. II-III with 7 and 6 central mac., respectively, Abd. I with 3-4 central mac., and cephalic groove (CG) and post medial labial (PLM) chaetotaxy (Table 1). Conversely, S. colombiana lacks dark-colored patterns on the body (present in S. thibaudi), and Ant. I with 7 mac. (4 in S. thibaudi), Abd. I with 2 + 2 or 3 + 3 central mac. (m2-4) anterior to S-microchaeta (ms) (4 + 4 in S. thibaudi), and Abd. IV with 8 + 8 lateral mac. (10 + 10 in S. thibaudi).

After the new species described here, Salina now has seven species of beta group from the New World, which can be identified in the following key.

Key to Nearctic and Neotropical species of Salina with rectangular mucro (in part, after Soto-Adames, 2010)

1. Abd. II with 2 + 2 central mac. (m3 and m3e) (Figs. 7 and 37) ... 2

1'. Abd. II with 1 + 1 central mac. (m3) ... 3

2. Th. II with 1 + 1 central mac. (p2); Th. III with 4 + 4 central mac. (p1, p2, p3 and p5) (Figs. 4 and 5); Brazil ... S. maculiflora sp. nov.

2'. Th. II with 7 + 7 central mac. (a5, m1, m2, m4, p1, p2 and p3); Th. III with 6 + 6 central mac. (p1, p2, p2a, p3, p3e and p5) (Figs. 34 and 35); Colombia ... S. colombiana sp. nov.

3. Abd. II and IV with dark and light blue transversal bands, respectively; Th. II with 4 + 4 central mac.; Th. III with 5 + 5 central mac.; USA ... S. betaChristiansen and Bellinger, 1980

3'. Abd. II and IV without transversal bands; Th. II with 3 + 3 to 8 + 8 central mac., but if 4 + 4 then Th. III with 4 + 4 or less mac. ... 4

4. Th. II to Abd. I with mac. formula 5, 5, 3; Cuba ... S. ventricolor Gruia, 1983

4'. Th. II to Abd. I with mac. formula never 5, 5, 3 ... 5

5. Th. II-III with 3 + 3 to 5 + 5 and 2 + 2 to 4 + 4 central mac., respectively, general formula 3, 4; collophore with 1 + 1 posterior chaetae; Puerto Rico ... S. wolcottiFolsom, 1927

5'. Th. II-III with 5 + 5 or more central mac.; collophore with 2 + 2 to 6 + 6 posterior chaetae ... 6

6. Prelabral chaetae two; Th. III with 5 + 5 to 6 + 6 central mac.; collophore with 2 + 2 posterior chaetae; Costa Rica and USA ... S. bidentata (Handschin, 1927)

6'. Prelabral chaetae four; Th. III with 5 + 5 to 9 + 9 central mac.; collophore with 3 + 3 to 6 + 6 posterior chaetae; Costa Rica ... S. thibaudiSoto-Adames, 2010

Acknowledgements

We thank Bruno Garcia Oliveira and other collectors from INPA for providing specimens for this study. Fernando Fernández (UNAL) for the loan of material from Colombia. Marlon B.C.S. da Graça for the help with English. Access to equipment and additional funding from CAPES Pro-Equipamentos. Neusa Hamada/CNPq, Laboratório de Sistemática e Ecologia de Invertebrados do Solo (Elizabeth F. Chilson), CBio, INPA, and Laboratório de Biologia Comparada e Abelhas (Eduardo A. B. Almeida) from USP. The first author is granted by FAPESP, São Paulo Research Foundation, #2013/26335-9/#2011/09477-9. The second author is granted a fellowship by CNPq.

References

• Arlé, R., Mendonça, M.C., 1982. Estudo preliminar das espécies de Dicranocentrus Schött, 1983, ocorrentes no Parque Nacional da Tijuca, Rio de Janeiro (Collembola). Braz. J. Biol. 42, 41-49.
• Bellinger, P.F., Christiansen, K.A., Janssens, F., 2015. Checklist of the Collembola of the World, Available at: http://www.collembola.org (accessed 28.05.15).
  » http://www.collembola.org
• Christiansen, K., Bellinger, P., 1980. Part 3. Family Entomobryidae. The Collembola of North America North of the Rio Grande, vol. 1. Grinell College, Iowa, pp. 785–1042.
• Christiansen, K., Bellinger, P., 1998. The Collembola of North America. North of Rio Grande, A Taxonomy analysis. Grinnell College, Iowa.
• Fjellberg, A., 1999. The Labial Palp in Collembola. Zool. Anz. 237, 309-330.
• Folsom, J.W., 1927. Insects of the subclass Apterygota from Central America and the West Indies. Proc. U.S. Nat. History Museum 72, 1-16.
• Good, R., 1974. The Geography of Flowering Plants, 4th ed. Longman Group, United Kingdom.
• Jantarit, S., Satasook, C., Deharveng, L., 2013. The genus Cyphoderopsis Carpenter (Collembola: Paronellidae) in Thailand and faunal transition at the Isthmus of Kra in Troglopedetinae. Zootaxa 3721, 49-71.
• Jordana, R., Baquero, E., 2005. A proposal of characters for taxonomic identification of Entomobrya species (Collembola, Entomobryomorpha), with description of a new species. Abh. Ber. Naturkundemus. Görlitz. 76, 117-134.
• Kottek, M., Grieser, J., Beck, C., Rudolf, B., Rubel, F., 2006. World Map of the Köppen–Geiger climate classification updated. Meteorol. Z 15, 259-263.
• Mari-Mutt, J.A., 1987. Collembola from two localities near Buenaventura, Colombia. J. Kans. Entomol. Soc. 60, 364-379.
• Mitra, S.K., 1973. A revision of Salina MacGillivray, 1894 (Collembola: Entomobryidae) from India. Orient. Insects 7, 159-202.
• Mitra, S.K., 1993. Chaetotaxy phylogeny and biogeography of Paronellinae (Collembola: Entomobryidae). In: Records of the Zoological Survey of India. Occasional Papers 154.
• Mitra, S.K., Dallai, R., 1980. Studies of the genus Campylothorax Schött, 1893 (Collembola Entomobryidae Paronellinae) with the description of a new species from Zaire. Ital. J. Zool. 9, 273-321.
• Soto-Adames, F.N., 2008. Postembryonic development of the dorsal chaetotaxy in Seira dowlingi (Collembola, Entomobryidae); with an analysis of the diagnostic and phylogenetic significance of primary chaetotaxy in Seira Zootaxa 1683, 1-31.
• Soto-Adames, F.N., 2010. Review of the New World species of Salina (Collembola: Paronellidae) with bidentate mucro, including a key to all New World members of Salina Zootaxa 2333, 26-40.
• Soto-Adames, F.N., Taylor, S.J., 2013. The dorsal chaetotaxy of Trogolaphysa (Collembola, Paronellidae), with descriptions of two new species from caves in Belize. Zookeys 323, 35-74.
• Szeptycki, A., 1979. Chaetotaxy of the Entomobryidae and its Phylogenetical Significance. Morpho-systematic Studies on Collembola. IV. Polish. Academy of Sciences, Kraków.
• Yoshii, R., 1981. Paronellid Collembola of Sabah. In: Entomological Report from the Sabah Forest Research Centre, No. 3, pp. 1–51.
• Yoshii, R., 1983. Studies on Paronellid Collembola of East Asia. In: Entomological Report from the Sabah Forest Research Centre, No. 7, pp. 1–28.
• Zhang, F., Deharveng, L., 2015. Systematic revision of Entomobryidae (Collembola) by integrating molecular and new morphological evidence. Zool. Scr. 44, 298-311.
• Zhang, F., Sun, D.-D., Yu, D.-Y., Wang, B-X., 2015. Molecular phylogeny supports S-chaetae as a key character better than jumping organs and body scales in classification of Entomobryoidea (Collembola). Sci. Rep. 5(2471), 1-12.

Publication Dates

• Publication in this collection
  Apr-Jun 2016

History

• Received
  27 July 2015
• Accepted
  03 Jan 2016