Systematics and biogeography of Salina MacGillivray (Collembola: Entomobryoidea), with emphasis on the species groups in the New World Author Oliveira, Fábio G. L. Author Cipola, Nikolas G. Author Almeida, Eduardo A. B. text Insect Systematics & Evolution 2020 2020-01-02 51 81 138 journal article 10.1163/1876312X-00002201 63257f64-79ba-4237-86d2-151af268a7c7 1876-312X 3786728 ABEAF11E-128B-4EC9-A3A9-94A2B7D08165 Salina brasiliana sp.n. Oliveira & Cipola Figures 9A , 10A , 11A , 12A , 13A , 14A and D , 15A , 16A , 17 A-B, 19C-D ZooBank: http://zoobank.org/ 59302B93-840D-486D-AC8C-4A0670BE519B 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. 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 . Diagnosis Body and legs with blue spots; Ant I with 4 mac; cephalic groove with 2 serrated mic, without smooth chaetae; Th II–Abd I with 1, 2, 2 central mac, respectively; Abd III with 6 lateral mac ( a7 , am6 , pm6 , p6 , p7i and one unnamed); Abd IV with 10 central mac ( A3–5 absent), and 10 lateral mac; collophore with 10 anterior, 3 posterior and 11 lateral flap chaetae; trochanteral organ with 12 spine-like chaetae; manubrial plate with 3 chaetae. Type material Holotype ♀ on slide (COLLE 042/INPA): Brazil , Tocantins , Palmas municipality, Taquaruçu district , ecological farm of “Taquaruçu”, 10°15’S , 48°08’W , Cerrado biome, 650 m , 13-20.v.2013 , Pitfall-trap , AS Lopes coll. Paratypes on slides (COLLE 042A- F/INPA): 4 ♂ and 2 ♀ , same data as holotype . Additional examined material 2 ♂ on slides and 3 specimens in alcohol (INPA): Brazil , Amapá , Oiapoque municipality, margin of stream next to the airport, 03°52’13”N , 51°47’30”W , Amazon forest , 22 m , 08-09.viii.2013 , Pitfall-trap , JMC Nascimento & N Hamada coll. 1 ♂ on slide and 1 specimen in alcohol (INPA): Roraima , Caracaraí , National Park of “Mocidade”, 01°36’N , 61°54’W , Amazon forest , 600 m , 15-26.i.2016 , Malaise-trap , R Boldrini & P Barroso coll. 1 ♂ and 1 ♀ on slide and 5 specimens in alcohol (INPA): National Park of “Viruá”, grid L2-2500, 01°28’39”N , 61°01’29”W , Amazon forest , 73 m , 21-29.v.2015 , Malaise-trap , SS Gadelha coll. 1 ♀ on slide (INPA), Caroebe municipality, margin of stream “Caroebe”, 00°54’48.5”N , 59°34’20”W , Amazon forest , 156 m , 19.iii.2013 , Manual , JMC Nascimento coll. 2 ♀ on slide and 7 specimens in alcohol (INPA), Acre , Rio Branco municipality, Zoobotanical Park of Universidade Federal do Acre , 09°57’23”S , 67°52’16”W , Amazon forest , 170m , 14-19.xii.2012 , Malaise-trap , SS Gadelha coll. 1 ♂ on slide and 2 specimens in alcohol (INPA): Senador Guiomard municipality, “São Francisco” farm, BR 317, km 14, 10°05’41”S , 67°38’17”W , Amazon forest , 211m , 13-27.vii.2014 , Malaise-trap , DRR Fernandes & DF Nogueira coll. 1 ♀ on slide and 1 specimen in alcohol (INPA): Manoel Urbano municipality, State Park “Chandless”, grid T1-500-1500, 09°23’52”S , 69°54’58”W , Amazon forest , 215m , 09°23’52”S , 69°54’58”W , Pitfall-trap , IPS Santos coll. 1 ♂ and 2 ♀ on slide (INPA): Alagoas , Maceió municipality, Parque Municipal de Maceió , 09°36’S , 35°45’W , Atlantic forest , 32m , xi.2010 , Pitfall-trap , IPS Santos coll. 1 ♂ and 1 ♀ on slide and 7 specimens in alcohol (INPA): Amazonas , Manaus , INPA, Campus II , 03°05’49”S , 59°59’19”W , urban forest, 70 m , 01-03.vi.2013 , Malaisetrap , GC Tavares coll. 1 ♂ and 1 ♀ on slides (INPA): “Embrapa Amazônia Ocidental”, 02°53’42.18”S , 59°59’10.58”W , cultivation of organic guaraná, 97m , 23.ix.2012 , Moerick-trap, K Schoeninger coll. 1 ♂ and 1 ♀ on slides (INPA): Reserva Ducke , sede, 02°55’S , 59°58”W, Amazon forest , 83m , 30.iv.2013 , yellow plate trap , NG Cipola coll. 2 ♂ and 2 ♀ on slides and 3 specimens in alcohol (INPA): Experimental farm of the Universidade Federal do Amazonas , grid L1-4500, 02°39’11”S , 60°06’08”W , Amazon forest , 71m , 06-18.viii.2010 , Pitfall-trap , C Brito & JLP Souza coll. 2 ♀ on slide and 11 specimens in alcohol (INPA): Reserve of Biological Dynamics Project of Forest fragments (PDBFF), road AM-174, km 41, 02°38’S , 60°11’W , Amazon forest , 87m , 12-13.vii.2004 , suspended trap , R Querino coll. 1 ♀ on slide (INPA): Reserve “ZF2”, path of the observation tower, 02°35’21”S , 60°06’55”W , Amazon forest , 122m , 12-13.vii.2004 , sweeping, JT Câmara & JA Rafael coll. 1 ♂ , 1 ♀ and juvenile on slide (INPA): Presidente Figueiredo municipality, Waterfall of “Maroca”, road AM-270, km 18, 02°00’08”S , 59°52’04”W , Amazon forest , 152m , 30.viii.2014 , entomological aspirator, NG Cipola & FGL Oliveira coll. 2 ♀ on slide and 1 specimen in alcohol (INPA): Cave Trail of “Maroaga”, road AM-270, km 06, 02°03’S , 59°58’W , Amazon forest , 140m , 31.viii.2014 , entomological aspirador, FGL Oliveira coll. 1 ♂ on slide (INPA): path of “Castanhal”, stream “Canoas”, 01°49’51”S , 60°04’15”W , Amazon forest , 124 m , 12.viii.2014 , sheet trap , AMO Pes coll. 2 ♂ and 1 ♀ on slide and 1 specimen in alcohol (INPA), Novo Airão municipality, Mato Grosso stream, 02°49’00”S , 60°55’08”W , Amazon forest , 36 m , 28-31.iii.2013 , dish trap , JT Câmara & AC Maldaner coll. 1 ♂ and 1 ♀ on slide and 28 specimens in alcohol (INPA): Rio Preto da Eva municipality, farm “Aprisco Pásargada”, forest margin, 02°42’26.6”S , 59°42’53.2”W , Amazon forest , 49m , 13.ix.2013 , suspended trap , BG Oliveira coll. 1 ♂ on slide (INPA), Barcelos municipality, sanctuary “Santo Alberto de Trapani”, between “Negro” river and “Caures” stream, 01°19’38.5”S , 62°06’52.2”W , Amazon forest , 13m , 13.xii.2012 , Pitfall-trap , JMC Nascimento coll. 2 ♂ , 1 ♀ and 1 juvenile on slide (INPA): Altazes municipality, farm next “Madeira” river, 03°40’33.9”S , 59°06’10.7”W , Amazon forest , 24m , 25.xii.2011 , Malaise-trap , GPS Dantas coll. 2 ♂ and 2 ♀ on slide and 16 specimens in alcohol (INPA), Tapauá municipality, Porto Cotinha in stream “Ipixuna”, 03°26’53”S , 64°40’57”W , Amazon forest , 73m , 08- 13.x.2013 , Malaise-trap , DMM Mendes coll. 2 ♀ on slide and 85 specimens in alcohol (INPA): Canutama municipality, Extractive Reserve “Canutama”, “Purus” river, 06°32’S , 64°22’W , Amazon forest , 52m , 01-10.iv.2013 , Malaise-trap, A Somavilla & M Oliveira coll. 1 ♀ on slide (INPA), idem , except 27-30.iv.2013 , yellow plate trap . 1 ♂ and 1 ♀ on slide and 21 specimens in alcohol (INPA): Maués municipality, farm “ Santa Helena ”, near guaraná cultivation, 03°27’13”S , 57°39’01”W , Amazon forest , 23m , 25-28.iv.2017 , Malaise-trap , A Somavilla coll. 1 ♂ on slide (INPA): Rondônia , Porto Velho municipality, Instituto de Pesquisas em Patologias Tropicais - IPEPATRO, road BR-364, 08°46’45”S , 63°51’57”W , urban area, 87 m , 03-04.i.2014 , Pitfall-trap , AM Pereira Jr coll. 2 ♀ on slide and 11 specimens in alcohol (INPA): Cacaulândia municipality, waterfall trail “Jamari”, 10°13’26.8”S , 63°13’49”W , Amazon forest , 120m , 10.ii-20.v.2012 , Malaise-trap , S Nihei & team coll . 1 ♂ and 2 ♀ on slides (MNRJ): Pernambuco , São Lourenço da Mata municipality, “Pau Ferro”, 07°58’S , 34°58’W , Atlantic forest , 107m , 27.iii.1978 , aspirator, MC Mendonça coll. 1 ♀ on slide (INPA): Minas Gerais , São Roque de Minas municipality, National Park Serra da Canastra , 20°09’S , 46°39’W , Cerrado biome, 1.250 m , xi.2011 , Malaise-trap . 1 ♂ and 2 ♀ on slide (MNRJ): Rio de Janeiro , São Gonçalo , Colubandê , 22°50’S , 43°00’W , Atlantic forest , in grass and plants, 30m , 14.iv.1957 , R Arlé coll. 5 ♂ and 3 juveniles on slide (INPA): Paraná , Cornélio Procópio municipality, State Park “Mata São Francisco”, 23°09’20”S , 50°34’20”W , Atlantic forest , 531m , 19.ix.2009 - 18.iii.2010 , Pitfall-trap , NG Cipola coll. 4 ♀ on slide and 19 specimen in alcohol (INPA): Santa Catarina , Orleans municipality, margin of “Mirador” stream, 28°10’43”S , 49°24’34”W , Atlantic forest , 420m , 15.ii-19.viii.2013 , Malaise-trap , LC Pinho , AL Schlindwein & AP Amaral coll. 1 ♀ on slide (INPA): Grão Pará municipality, State Park “Serra Furada”, 28°07’48”S , 49°25’25”W , Atlantic forest , 678m , 7.v-9.vi.2013 , Malaise-trap , LC Pinho , AP Amaral , MO Bessel & AM Will coll. 2 ♂ and 6 ♀ on slide (MZUSP): São Francisco do Sul municipality, villa of “Glória”, 26°13’S , 48°40’W , Atlantic forest , 7m , 14-20.x.2001 , Malaise-trap . 2 ♂ , 4 ♀ and 1 juvenile on slides and 22 specimens in alcohol (UNAL): Colombia , Guaviare , San José del Guaviere municipality, Playa Guio , 02°34’N , 72°43’W , Amazon forest , 191 m , 12-19.iv.2013 , Malaise-trap , Animal Systematic students coll . Description Total length (head + trunk) of holotype 1.75 mm. Specimens pale white with dark blue pigments on Ant I–IV, strongly on anterior head, intersegmental areas of antennae and Th II to Abd III ; irregular blue spots on the side of the head, Th II and Abd II–V; inner side of legs with a distal spot on femora and two spots in tibiotarsi (one basal and one subapical). Eyepatches black ( Figure 9A ). Head. Ant I dorsally with 4 mac and 5 basal spiny smooth mic ( Fig 10A ). Posterior labial chaetotaxy series ‘CG’ with 7 ciliate chaetae ( CG 1-3 , CG 5 , CG 6p–7e ) and 2 serrated mic ( CG 4 , CG 6 ); series ‘PLM’ with 2 ciliate chaetae ( PLM 1–2 ); series ‘PLE’ with 2 ciliate chaetae ( PLE 1–2 ); lateral side with about 29 ciliate chaetae ( Fig 11A ). Dorsal chaetotaxy. Th II with 1 ‘p’ mac ( p3 ). Th III with 3 ‘p’ mac ( p2–3 , p5 ) ( Figure 12A ). Abd I with 1–2 ‘m’ mac ( m3 , m4 ), m3 rarely absent ( Figure 13A ). Abd III with 1 ‘a’ mac ( a7 ), 2 ‘m’ mac ( am6 , pm6 ), and 3 ‘p’ mac ( p6 , p7i and one unnamed) ( Figure 14A ). Abd IV with 2 ‘A’ mac ( A1 , A6 ); 1 ‘Ae’ mac ( Ae1 ); 3 ‘B’ mac ( B3–5 ); 1 ‘Be’ mac ( Be1 ); 1 ‘C’ mac ( C1) ; 4 ‘E’ mac ( E1-4 ); 4 ‘F’ mac ( F1–F3p ); 2 ‘Fe’ mac ( Fe1–3 ); posterior side with 3 sens type IV ( ps and two unnamed) ( Figure 14D ). Abd V with 2 ‘a’ mac ( a3 , a5 ); 3 ‘m’ mac ( m2–3 , m5 ); and 5 ‘p’ mac ( p0-4 ) ( Figure 15A ). Appendages. Trochanteral organ with 12 smooth spine-like chaetae ( Fig 16A ). Collophore anterior side with 2 subapical mac of unequal length and 1 median mes, and 7 proximal smooth mic; posterior side with 1 apical and 2 subapical smooth chaetae; lateral flap formula 4(s), 2(m), 5(i) smooth chaetae, 2 inferior larger ( Figures 17 A-B). Manubrial plate with 3 chaetae ( Figure 19C ). Mucro with 3–4 teeth ( d1 , ap , v1-2 ), v2 teeth present or absent ( Figure 19D ). Etymology The name “brasiliana” refers to the wide distribution of this species in Brazil . Remarks Salina brasiliana sp.n. resembles the different forms of S. celebensis Schäffer, 1898 , widely recorded in South Asia, by body color with dark blue spots on trunk and legs, dorsal chaetotaxy of Th II–Abd I with 1, 2, 2 central mac, respectively, Abd II with 2, 1 mac, prelabral and labral chaetotaxy, maxillary outer lobe and sublobal plate, basolateral and basomedian labial fields, unguiculus truncate, and mucro with 3 teeth (see Schäffer 1898 ; Handschin 1925 ; Denis 1936 ; Yosii 1959 ; Yoshii 1981 , 1983 ; Yoshii & Suhardjono 1989 ; Yoshii & Greenslade 1993 ). However, S. brasiliana sp.n. differs from S. celebensis from Celebes ( type locality), by spots on trunk and legs (only one lateral strip on Th II of S. celebensis ), and mucro generally with v2 teeth present (absent in S. celebensis ), being that this last characteristic is not present in differents forms of S. celebensis from Asia (see Table 2 ). Salina brasiliana sp.n. also differs from specimens 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. Table 2. Comparison (per side) among Salina species with 2 ( m3 and m3e ), 1 ( m5 ) macrochaetae on Abd II, truncate unguiculi and mucro square.

Morphological characteristics
Body	Ant. I	Prelabral	Th II	Th III	Abd I Abd IV	Collophore		Trocanteral	Number of
Species	color pattern	DM	chaetae	CM	CM	CM central lateral mac mac	anterior	lateral flap	posterior	organ chaetae	mucronal teeth
(s, m, i)
S. banksi ¹, ⁷, ¹^	longitudinal bands	6	4	8	6	2 8?	?	?	8	?	3
USA
S. bellinii sp.n.	restricted on the	3–4	4	2–5	5–9	2–4 8 10	3C;4S	2, 3, 5	2S	13	3–4
BR	side
S. bicolor sp.n.	longitudinal bands	4	4	1	2	2 7 9	3C;4S	4, 5, 5	4S	12	4
CO
S. brasiliana sp.n.	irregular	4	4	1	2	2 (1, 3) 8 10	3C;7S	4, 2, 5	3S	12	3–4
CO, BR	spots
S. celebensis ³, ¹¹,	irregular	?	4	1	2	2 10 4?	?	?	?	18	3
¹², ¹⁵, ¹⁷, ¹⁸, ²⁰, ²¹	spots or reduced
IND S. choudhurii ¹⁰	transverse and	?	4	2	4	3 8 7	?	?	?	30	3
IND	longitudinal bands
S. dedoris ⁸, ⁹, ¹^	transverse bands	4	4	6	8	3 (4) 8 7	3C;4S	4, 4, 5	0–2S	12	4
BR, CO S. greensladeae ²⁰, ²¹	longitudinal bands	?	4	1	2	2??	3C;8S	?	6C	20	3
INS S. griscescens ¹⁶	irregular	?	?	6	11	3??	?	?	?	25	3
THA	spots
S. javana ^, ¹⁰	transverse and	?	4	9–10	9–10	5??	4C;7–9S	?	?	24	3
IND	longitudinal bands
S. hamadae sp.n.	irregular	9	4	1–2	3	2 10 9	4C, 4S	4, 4, 4	4S,1C	16	3
BR	spots
S. hermana ⁹	irregular	4	4	6	8	3 8 7	3C;4S	4, 4, 5	0–2S	12	4
CO	spots on
Abd IV

S. maculipenis sp.n. penis-shaped spot		5	4	3–6 4–5 1–2			8	12	3C, 8S	4, 6, 5	2S	14	4
BR
S. moluccana ²²	irregular	?	4	10	9	5	?	?	?	?	?	?	3
INS	spots
S. montana ⁵, ¹⁰	U-shaped	?	?	8	6	4	?	?	4C; 7S	?	?	32	3
IND	spot on Th II –
Abd I
S. okinawana ¹⁸	transverse bands	?	?	2	3	2	?	?	?	?	?	?	3?
JP
S. oceanica ¹⁹, ²²	reduced	?	2	4–5	5–6	2–3	?	?	2C; 6C	20	?	50	4
NC
S. panamae ⁶, ⁸, ¹^	reduced	?	?	1	3	2	8	?	?	?	?	12	4
PAN
S. peruana sp.n.	reduced	3	4	1	1	1	7	9	3C, 4S	5, 2, 5	1S	14	3
PER
S. serrana sp.n.	irregular	7	4	1	2	2 11–12		10	3C, 10S 5, 6/4, 5		4S	13	3
BR	spots
S. trilobata ¹³, ¹^	longitudinal band	?	?	?	?	?	?	?	?	?	?	?	3
MEX
S. tristani ², ⁸, ⁹,	restricted on the	4	4	6–8	6–10 2–6		8	7	3C, 5S 6, 5, 4–5		4–5	13	4
¹^, ²³	side
CR, PR , BR
S. tocantinensis sp.n. restricted on the		4	4	3–4	3–6	1–2 (3) 8		10	3C, 4S	4, 4, 5	2S	13	3–4
BR	side
S. unisetosa sp.n.	reduced	3	4	1	1	1	8	10	3C, 5S	5, 5, 5	2S	15	3–4
BR

Abbreviations and symbols used to represent the morphological characteristics: DM=dorsal macrochaeta; CM=dorsal macrochaeta; C=ciliated chaeta; S=smooth chaeta; s=superior; m=median; I=inferior; BR= Brazil ; CO= Colombia ; CR= Costa Rica ; INS= Indonesia ; IND= India ; JP= Japan ; NC= New Caledonia ; PAN= Panama ; PER= Peru ; PR= Puerto Rico ; THA= Thailand ; USA = United States ;?=unknown, ()=exceptional chaetal variation. Reference species: ⁽¹⁾ Christiansen & Bellinger 1998 ; ⁽²⁾ Denis 1931 ; ⁽³⁾ Denis 1936 ; ⁽⁴⁾ Handschin 1928 ; ⁽⁵⁾ Imms 1912 ; ⁽⁶⁾ Jacquemart 1982 ; ⁽⁷⁾ MacGillivray 1894 ; ⁽⁸⁾ Mari-Mutt 1987a ; ⁽⁹⁾ Mari-Mutt 1987b ; ⁽¹⁰⁾ Mitra 1973 ; ⁽¹¹⁾ Salmon 1957 ; ⁽¹²⁾ Schäffer 1898 ; ⁽¹³⁾ Schött 1896 ; ⁽¹⁴⁾Soto- Adames 2010; ⁽¹⁵⁾ Yosii 1959 ; ⁽¹⁶⁾ Yosii 1961 ; ⁽¹⁷⁾Yosii 1981; ⁽¹⁸⁾Yosii 1983; ⁽¹⁹⁾ Yoshii 1989 ; ⁽²⁰⁾ Yoshii & Greenslade 1993 ; ⁽²¹⁾ Yoshii & Suhardjono 1989 ; ⁽²²⁾Yoshii & Suhardjono 1992; ⁽²³⁾ Personal observation. of S. celebensis from Bukit Timah, Singapore ( sensu Yosii 1959 ) by unguis with inner median tooth (absent in S. celebensis ), trochanteral organ with 12 smooth spine-like chaetae ( 18 in S. celebensis ), Abd III with 6 lateral mac ( 1 in S. celebensis ), and Abd IV with 8 central mac ( 10 in S. celebensis ). Specimens of S. celebensis from Sabah and Malaysia has Abd III with 3 lateral mac and Abd IV with 10 central mac, as well as about the color pattern with or without spots on trunk, this may be considered a variation expressed in lineages close related to S. celebensis ( Yoshii 1981 , 1983 ). The new species still differs from specimens of S. celebensis from India ( sensu Denis 1936 ; Mitra 1973 ), by Th II–Abd I with 1, 2, 2 central mac, respectively (7, 5, 2 in S. celebensis ), besides of extra mucronal tooth ( v2 ), absent in S. celebensis . Salina brasiliana sp.n. also resembles other Neotropical species, S. panamae Jacquemart, 1982 , in general morphology, including the reduction of central mac on Th II–III and Abd IV with 8 central mac (see Jacquemart 1982 ; Soto-Adames 2010 ). However, S. brasiliana sp.n. differs from this species by the color pattern with irregular spots (reduced in S. panamae ), Th III without p1 mac (present in S. panamae ), and Abd III with 3 lateral mac ( am6 , pm6 , p6 ) next to m5 bothriotrichum ( 2 in S. panamae ). Thus, the formula of Th II–Abd I (1, 2, 2 central mac) is not exclusive of S. brasiliana sp.n. and S. celebensis , since it is also present in S. greenslade Yoshii & Suhardjono, 1989 , S. bicolor sp.n. and S. serrana sp.n. (see remarks of these new species). For this reason, identification based on formula Th II–Abd I, as well as color pattern, may not be accurate ( Soto-Adames 2010 ). Thus, the records of S. celebensis in Brazil and Argentina ( Cassagnau 1963 ; Soto-Adames 2010 ), probably refers to S. brasiliana sp.n. The populations of S. brasiliana sp.n. have similar variations independently of the region from Brazil . Specimens in general have two central mac on Abd I ( Figure 13A ), but frequently m3 mac is absent on at least one body side in specimens from North Brazil ( Acre , Amapá , Amazonas, Roraima and Rondônia States). In this same region the specimens often have 3 or 4 mucronal teeth, in both or only in a dens, whereas in the specimens from South Brazil ( Paraná and Santa Catarina states) has greater tendency of 3 mucronal teeth ( v2 absent). In Abd IV rarely Ae3 is mac/mes, at least in specimens from Amazonas and Acre states, but this may be related to the development stage.