Salina MacGillivray, 1894

Oliveira, Fábio G. L., Cipola, Nikolas G. & Almeida, Eduardo A. B., 2020, Systematics and biogeography of Salina MacGillivray (Collembola: Entomobryoidea), with emphasis on the species groups in the New World, Insect Systematics & Evolution 51, pp. 81-138 : 86-95

Salina MacGillivray, 1894

Diagnosis

Body scales absent, with ciliated mac apically clavate or acuminate, and mic apically branched ( Figures 1A , D–F, 2A, 6, 9); antennae in adults subequal or larger than body length and with 4 segments ( Figure 9 ); 8 eyes per side, with 3 interocular chaetae; tergal chaetotaxy polychaetotic or oligochaetotic; head ‘An’ series with An2a serrated mic and ‘S’ series with 2+2 (S2 and S3) mac in trapezium-shaped ( Figures 2A , C–D, 9A, F); basolateral labial field with chaetae a5 smooth and thicker ( Figures 3E , 10M ); Abd II–IV bothriotricha formula 2, 3 and 5 (3 of them as secondary bothriotricha); ms and sens formula of Th II–Abd V as 1, 0| 1, 0, 1, 0, 0 and 1, 1| 0, 0, 1, +, 3, respectively ( Figures 1 H–M, 6–8); Th II with or without central mac; Th III with at least one central mac (p3); Abd IV 2.5 to 4 times the length of Abd III in the midline ( Figure 8 ); males with papilate genital plate; females with four smooth chaetae surrounding the genital opening ( Figure 19 A-B); dentes smooth with one distal rounded dorsal appendix; mucro rectangular with 2–3 teeth or square with 3–4 teeth ( Figures 5 C-E, 19); (Adapted from Mitra 1973; Soto-Adames 2010; Zhang et al. 2015; Oliveira & Cipola 2016).

Morphological definition of celebensis group

Coloration. Variable according to the species, body generally yellowish white with irregular blue pigment on antenna, lateral areas of tergites and legs, or presence of

transverse and/or longitudinal bands of pigments; eyes darkly pigmented frequently on eyepatches ( Figure 9 ).

Cuticule. Hexagonal pattern formed by the connection of six primary triangular microgranules which are strongly united in ocellar lenses ( Figures 1B , 2B ).

Pseudopore. Small, with smooth surface present medially on Th II to Abd IV. They are subtle and difficult to observe with optical microscope ( Figures 1C , 7 B–E, 8A–B).

Tergal chaetae

Branched mic. Gradually spiral and apically branched, compound by filaments apically rounded, and present on dorsal body ( Figures 1F , 6 ). This chaeta is not used in the diagnosis of Salina , but this type of sculpture is typical of the genus.

Club mac. Long, densely ciliate, apically clavate (foot-like) present on dorsum of the head thorax and abdomen ( Figures 1D , 6 ).

Ciliate mac or mes. Long, apically acuminate and densely ciliate present on head, thorax and abdomen ( Figures 1E , 6 ).

Bothriotrichum. Basally smooth and strongly ciliate in its full length, moderately long present in the head and very long on Abd II–IV ( Figures 1G , 7E , 8 A–B, 14).

S-microchaeta (ms). Very small, slightly striated, apically clavate, present on lateral of Th II, Abd I and III ( Figures 1H , 6 , 7A, D , 8A , 12–13, 14A–C).

Sens type I (al = anterolateral sens). Rather long, smooth and apically pointed present on lateral of Th II–III ( Figures 1I , 6 , 7 B–C, 12).

Sens type II (as = anterosubmedial sens). Small, smooth and apically rounded finger-like present on Abd III and Abd V ( Figures 1J , 6 , 8A, C , 14A–C, 15).

Sens type III (acc.p = accessory sens). Smooth, apically thinner and gently acuminate present on Abd V ( Figures 1K , 6 , 8C , 15).

Sens type IV (ps = posterior sens and unnamed sens). Long and smooth, apically rounded finger-like present on postero-median side of Abd IV generally in number of three-four ( Figures 1L , 6 , 8B , 14D–I).

Sens type V (bs = bothriotrichal sens). Small and ramification formed by four mediodistal filaments, present between T2 and T4 bothriotricha ( Figures 1M , 6 , 8B , 14D–I).

Serrated mic. Small, flexible, and with medio-distal ramifications of about nine filaments apically pointed. They are in antennal series (An2) of dorsal head and on ventral cephalic groove (CG5) ( Figures 2 C–D, 6, 7A, 11).

Head. Antennae 1.2 times or more than body length ( Figure 9 ); Ant IV weakly annulated with a simple apical bulb retractile, numerous finger-shaped sens and two types of ciliate chaetae: thin with short cilia and thick with longer cilia ( Figures 2 E–F). Ant III with an apical organ apically rounded, compound by three acuminate guard sensillae (one is not evidenced in the figure), some rods and finger-shaped sens, and many thick chaetae with longer cilia ( Figure 2G ). Ant I dorsally with variable number of mac, about 3–9, and 4–6 basal spiny smooth mic ( Figure 10 A–I). Eyes oval, ocelli G and H smaller, others subequal ( Figures 2A , 7A ). Oligochaetotic macrochaetotaxy; ‘An’ series with five mac (An1a–1, An2–3) and one serrated mic (An2a); ‘M’ series with two chaetae, M4 mac, M2 mes; ‘S’ series with three chaetae, S2 and S3 mac, S7 mes; ‘Ie’ series with three chaetae, r as mac, p and t as mic; ‘Ps’ series with three mes (Ps2–3, Ps5); ‘Pa’ series with two mac (Pa5, Pa5a) and one bothriotrichum (Pa6); ‘Pm’ series with two mac (Pm1, Pm3); ‘Pp’ series with one mac (Pp3); and ‘Pe’ series with one mac (Pe3) ( Figure 7A ). Four labral papillae, inner papillae square, and outer papillae larger and triangle-shaped ( Figures 3C , 10J ). Four prelabral ciliate chaetae (except Salina oceanica Yoshii 1989 , with two) ( Figures 3A , 10J ). Labral formula with 4 (a1–2), 5 (m0–2), 5 (p0–2) smooth chaetae, a1 thicker and finger-shaped apically, posterior row gently larger, others subequal ( Figures 3 A–B, 10J). Basomedian and basolateral labial fields with chaetae M (can be smooth in S. zhangi Bellini & Cipola, 2017 ), E, L1-2 ciliate, a1-5 smooth, a5 thicker, chaetae r absent ( Figures 3E , 10M ). Labial palp with five main papillae (A–E) plus one hypostomal papilla (H), with 0, 5, 0, 4, 2, 2 guard appendages (e3 and e6 absent), respectively; lateral process (l.p.) of papillae E finger-shaped and not reaching the papilla basis; labial palp with 5 or 4 (rarely) smooth proximal chaetae (p.c.) ( Figures 3E , 10L ). Maxillary outer lobe with one apical appendage (a.a.) lightly denticulate, and one thick subapical chaetae (b.c.) more denticulate, both weakly acuminate apically with the same length; sublobal plate with three smooth appendages ( Figures 3A, D , 10K ). Posterior labial chaetotaxy ( Figure 11 ); series ‘CG’ with 6–11 chaetae, CG1–2 and CG7 ciliate, CG4 and CG6 serrated mic or ciliate chaetae, other smooth or ciliate chaetae; series ‘PLM’ with one to three ciliate chaetae (PLM1–2); series ‘PLE’ with one or two ciliate chaetae (PLE1–2).

Thorax dorsal chaetotaxy. Th II ( Figure 7B ); ‘m’ series with 1–2 mac (m1, m7) often present; ‘p’ series with 0–8 mac (p1i–1a, p2–5), 1 S-microchaetae (ms) and 1 sens type I (al). Th III ( Figure 7C ); ‘a’ series with or without mac (a7); series ‘m’ with 1 mac (m7); ‘p’ series with 1–11 mac (p1ip–p1p, p2p–2a, p3–3p, p4–5), p3 always present, and 1 sens type I (al).

Abdomen dorsal chaetotaxy. Abd I ( Figures 7D , 13A-I); ‘a’ series with 0–3 mac (a1–3); ‘m’ series with 1–3 mac (m2–4), 1 always present (m3 or m4) and 1 S-microchaeta (ms). Abd II ( Figure 7E ); ‘a’ series with 1 bothriotrichum (a5), a6 absent; ‘m’ series with 4 chaetae, m3–3e and m5 as mac, m2 as bothriotrichum; ‘p’ series with 2 chaetae (p6–7), and el chaeta present. Abd III ( Figures 8A ); ‘a’ series with 1–2 chaetae, a7 as mac and a5 as bothriotrichum; series ‘m’ with 4 chaetae, pm6 as mac, am6 mac or mes, and m2 and m5 bothriotricha; series ‘p’ with 2–4 chaetae (p6, p7i and two unnamed chaetae); 1 S-microchaetae (ms) and 1 sens type II (as). Abd IV ( Figures 8B ); ‘A’ series with 2–6 chaetae (A1, A3–6); ‘ Ae’ series with 1 chaetae (Ae1) present or absent; ‘B’ series with 4 chaetae, B3–5 as mac and B6 as bothriotrichum; ‘ Be’ series with 1 mac (Be 1); ‘C’ series with 1 mac (C1); ‘T’ series with 2 bothriotricha ( T2 and T4 ); ‘E’ series with 4 chaetae (E1–4); ‘F’ series with 4 chaetae (F1–3p); Fe’ series with 4–6 chaetae, Fe 1–3, Fe 6 as mac (or Fe 3 and Fe 6 as mes), Fe 4–5 as bothriotricha; posterior side with 1 sens type III (ps), 2–3 sens type IV, and 1 sens type V (ts) between the bothriotricha T2 and T4 . Abd V ( Figures 8C ); series ‘a’ with 2–4 chaetae (a0, a3, a5–6), a5–6 always present; series ‘m’ with 2–5 chaetae (m0, m2–3, m5–5a), m2 and m5 always present; series ‘p’ with 4–8 chaetae (p0, p1–5, ap6 and pp6), p1, p3–4 always present; and 3 sens type II (as, acc.p4 and acc.p5).

Legs. Trochanteral organ with variable number of short smooth spine-like chaetae (between 10 and 20 in Neotropical species) on inner side of trochanter ( Figures 16 A–I). Tibiotarsi inner side with an apical monocondyle socket; tibiotarsus III with one striated inner subapical chaeta larger than unguiculus. Tibiotarsi outer side with one distal tenent hair longer than unguis ( Figures 4 A–B, D, 16J–K). Tenent hair dorsally excavated, apically capitate and strongly ciliate by finger-shaped cilia ( Figures 4 A–B, F–G). Pretarsi posteriorly with one minute smooth chaeta, chaeta absent on anterior side ( Figures 4 C–D, 16J–K). Ungues outer side longitudinally striated and with a pair of basolateral teeth; inner side with 4 teeth, one pair of basal teeth, and two unpaired teeth (median and distal). Unguiculi with truncate inner lamella, outer lamellae acuminate with smooth edge ( Figures 4 A–E, 18J–K).

Collophore. Anterior side generally with 2–4 subapical long ciliate mac and 4–10 proximal smooth mic; posterior side with up to 8 smooth (common) or ciliate chaetae, apical chaetae larger; lateral flap with smooth chaetae with 3 transverse rows (except Salina serrana sp.n. with 4 rows): superior, median and inferior (generally larger) ( Figures 5A , 17–18 ).

Tenaculum ( Figure 5B ). Basal corpus with one long median striated chaetae, one pair of rami with 4 outer distal teeth, and two inner prehensile projections.

Male genital plate ( Figure 19A ). Papillate and with 7+8 smooth chaetae surrounded by a papilla, 4 superior and 1 inferior pin-like chaetae, 1 superior bulb-like chaetae and 3 lateral robust spine-like chaetae; inner side with 3 small smooth eugenital chaetae per side, near the genital opening. Female genital plate ( Figure 19B ): anterior and posterior lobes separated by genital opening, both with one pair of smooth chaetae.

Furcula. Manubrium with smooth edges and ciliate chaetae; distally with one long lateral chaetae; manubrial plate with 2–3 ciliate chaetae and 1 psp ( Figure 5C and 19C ). Dentes smooth and with ciliate chaetae, without crenulation and spines; dorsal side with one apical oval appendix associated to an insert excavation, apical appendix smaller than mucro ( Figures 5 C–E, 19C). Mucro square or slightly rectangular with 3 main apical teeth (d1, ap and v1) and one subapical accessory tooth present or absent (v2) on a dorsal excavation; base to apex of mucro striated in ventral and dorsal edges ( Figures 5 D–E, 19D–I).

Remarks

Salina may have an additional characteristic useful to be differentiated from Akabosia . The labial papilla E in Salina species ( Figures 3E , 10L ) has two guard appendages (e1 and e2), and this certainly is typical of the genus (Mari Mutt 1987a; Oliveira & Cipola 2016; Bellini & Cipola 2017), since Akabosia has four guard appendages (e3 and e6 present) (see Kang & Park 2013). The morphology of male genital plate of Salina ( Figure 19A ) is probably other typical characteristic of the genus, previously observed by Handschin (1925), Yosii (1959), Gruia (1983), Mari Mutt (1987a) and Yoshii & Greenslade (1993). However, in description of Yosii (1959), the genital plate has superior spatulate chaetae, at least in S. celebensis , but in the Neotropical species, there are pin-like chaetae (Mari Mutt 1987a), except Salina ventricolor Gruia, 1983 which is more similar to S. celebensis .

The long lateral chaeta present distally in manubrium may be another characteristic of Salina , since it is present in all species analyzed in this study. Thus, these structures should be investigated in Salina species, as well as in Akabosia , to elucidate whether these characters are diagnostic at species or genus level.

Descriptions of new species

The morphological characteristics shared by the new species of Salina species belonging to the celebensis group will not be repeated in the following descriptions (see morphological definition of celebensis group, the figures 1A-M, 2A-G, 3A-E, 4A-G, 5A-E, 6, 7A-E, 10J-M, 19A-B and Table 2 ).

Figures

Fig. 1. Salina serrana sp.n., habitus and tergal structures:(A) lateral habitus; (B), cuticle and ecdysial line; (C), pseudopore; (D), mac apically clubed; (E), mac apically acuminate; (F), mic apically branched; (G), bothriotrichum of Abd II (basal region); (H), S-microchaeta (ms) of Th II, Abd I and III; I, sens type I of Th II–III; (J), sens type II of Abd III; (K), sens type III of Abd V; (L), sens type IV of Abd IV; (M), sens type V (bs) present between T2 and T4 bothriotricha of Abd IV.

Fig. 9. Habitus of Salina spp. (dorsal view): (A), Salina brasiliana sp.n.; (B), S. bellinii sp.n.; (C), S. bicolor sp.n.; (D), S. hamadae sp.n.; (E), S. maculipenis sp.n.; (F), S. peruana sp.n.; (G), S. serrana sp.n.; (H), S. tocantinensis sp.n. (distal half of Ant IV missing); (I), S. unisetosa sp.n.; (J), S. dedoris from Roraima state, Brazil; (K), S. tristani from Amazonas state, Brazil. Scale bars: 0.5 mm.

Fig. 2. Salina serrana sp.n., antenna and head structures: (A), dorsal head, arrow indicates the “sutural series”; (B), lent of the D eye on right side (lateral view), yellow color indicates the differentiated cuticle; (C), dorsum of the Ant I base and anterior head, arrow indicates serrated mic of antennal series; (D), serrated An2a mic; E, apex of Ant IV, apical bulb not visible; (F), median part of Ant IV, arrow indicates annulations; (G), apex of Ant III, green marked indicates apical organ, orange marked indicates the ventro-external microsens, red marked indicates guard sensillae, and blue marked indicates the long finger-shaped sens. “For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.”

Fig. 3. Salina serrana sp.n., anterior head and mouthparts: (A), labral papillae, maxillary lobes, prelabral and labral chaetotaxy; (B), Chaeta a1 of labrum; (C), labral papillae; (D), maxillary outer lobe and sublobal plate appendages; (E), labial palp (a-e = labial papillae, h = hypostomal papilla) and labial basomedian (a1-2 smooth chaetae, M and E ciliate chaetae) and basolateral fields.

Fig. 10. Head structures of Salina spp.: (A–I), Ant I dorsal chaetotaxy (right): (A), Salina brasiliana sp.n.; (B), S. bellinii sp.n.; (C), S. bicolor sp.n.; (D), S. hamadae sp.n.; (E), S. maculipenis sp.n.; (F), S. peruana sp.n.; (G), S. serrana sp.n.; (H), S. tocantinensis sp.n.; (I), S. unisetosa sp.n., arrow indicates mac present or absent. (J–K), general structures of anterior and ventral head: (J), labral papillae, prelabral and labral chaetotaxy; (K), maxillary outer lobe and sublobal plate; (L), labial palp and proximal chaetae; (M), labial basolateral and basomedian fields.

Fig. 8. New proposal of tergal homology for the celebensis group: (A), Abd III; (B), Abd IV, arrow indicates sens rarely present, arrow two ends indicates variable positions of B3 mac; (von C), Brill. Abd com05 V.

Fig. 19. Genital plate and furcula of Salina spp.: (A–B), Genital plate of Salina serrana sp.n. (ventral view): (A), ♂; (B), ♀. (C), Distal manubrium and proximal dens of S. brasiliana sp.n. (lateral view), arrow indicates chaeta absent in manubrial plate of some species. (D–I), distal dens and mucro (inner view):(D), S. brasiliana sp.n.; (E), S. bellinii sp.n.; (F), S. hamadae sp.n.; (G), S. maculipenis sp.n.; (H), S. peruana sp.n.; (I), S. serrana sp.n.

Fig. 5. Salina serrana sp.n., abdominal appendages: (A), collophore (ventral view); (B), tenaculum (ventral view); (C), furcula (lateral view); (D), distal dens and mucro (internal view); (E), distal dens and mucro (posterior view).

Fig. 7. New proposal for tergal homology for the celebensis group (morphological terminology adapted from Szeptycki, 1979). (A), head; (B), Th II; (C), Th III; (D), Abd I; (E), Abd II.

Fig. 6. Symbols of chaetae used in chaetotaxy of Salina spp.

Fig. 11. Head ventral chaetotaxy of Salina spp.: (A), Salina brasiliana sp.n.; (B), S. bellinii sp.n.; (C), S. bicolor sp.n.; (D), S. hamadae sp.n.; (E), S. maculipenis sp.n.; (F), S. peruana sp.n.; (G), S. serrana sp.n.; (H), S. tocantinensis sp.n.; (I), S. unisetosa sp.n.

Fig. 16. Legs structures of Salina spp.: (A–I), trochanteral organ (right): (A), Salina brasiliana sp.n.; (B), S. bellinii sp.n.; (C), S. bicolor sp.n.; (D), S. hamadae sp.n.; (E), S. maculipenis sp.n.; (F), S. peruana sp.n.; (G), S. serrana sp.n.; (H), S. tocantinensis sp.n.; (I), S. unisetosa sp.n. (J–K), distal tibiotarsus and foot complex (posterior side): (J), fore leg; (K), hind leg.

Fig. 4. Salina serrana sp.n., legs structures: (A), distal tibiotarsus and foot complex I (anterior side); (B), distal tibiotarsus and empodial complex III (posterior side); (C), connection of empodial complex III (anterior side), arrow indicates paired external teeth; (D), connection of empodial complex III (posterior side), red arrow indicates posterior pretarsal chaeta, white arrow indicates inner smooth chaetae; (E), external side of distal tibiotarsus and unguis III; (F), tenent-hair III (laterodorsal view); (G), apical region of tenent-hair III. “For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.”

Fig. 17. Collophore chaetotaxy of Salina spp.: (A–B), Salina brasiliana sp.n.: (A), anterior side; (B), lateral and posterior side. (C–D), S. bellinii sp.n.: (C), anterior side; (D), lateral and posterior side. (E), complete chaetotaxy (lateral view) of S. bicolor sp.n. (F–G), S. hamadae sp.n.: (F), anterior side; (G), lateral and posterior side.

Fig. 18. Collophore chaetotaxy of Salina spp.: (A–B), Salina maculipenis sp.n.: (A), anterior side; (B), lateral and posterior side. (C–E), complete chaetotaxy (lateral view): (C), S. peruana sp.n.; (D), S. serrana sp.n.; (E), S. unisetosa sp.n.; (F–G), S. tocantinensis sp.n.: (F), anterior side; (G), lateral and posterior side.