Heteromurus (Verhoeffiella) gamae, Lukić, Marko, Porco, David, Bedos, Anne & Deharveng, Louis, 2015

Lukić, Marko, Porco, David, Bedos, Anne & Deharveng, Louis, 2015, The puzzling distribution of Heteromurus (Verhoeffiella) absoloni Kseneman, 1938 (Collembola: Entomobryidae: Heteromurinae) resolved: detailed redescription of the nominal species and description of a new species from Catalonia (Spain), Zootaxa 4039 (2), pp. 249-275 : 266-271

Heteromurus (Verhoeffiella) gamae sp. nov.

Figs 52 , 55, 58 , 60

Type material. Holotype: adult male on slide, Spain, Tarragona, Mola de Cati, Forat del Rastre (cave) (coordinates WGS 84 X =0.283331°, Y =40.799838°, alt. 1240 m.), 08.ii.2014, Carles Fontgivell Dalmau leg. (CLL 4559); paratypes: 1 subadult female on slide, 1 juvenile ex. in 96% alcohol, 08.ii.2014, Carles Fontgivell Dalmau leg. (CLL 4279); skins of 2 barcoded ex., 04.xii.2002., Arnaud Faille leg. (ETA-050); skin of 1 barcoded ex., 13.v.2003, Arnaud Faille leg. (ETA-052).

Type material deposition. Holotype and three paratypes (ETA-050, ETA-052) deposited in MNHN, Paris. Two paratypes (CLL 4279) deposited in CBSS, Zagreb, Croatia.

Etymology. The new species is named in honor of Maria Manuela da Gama, for her essential contribution to the knowledge of cave Collembola of the Iberian Peninsula.

Diagnosis. Color whitish or very pale orange. Scales present on dorsal and ventral side of body and dorsal side of head, on Ant. Ib and Ant. II, on legs, ventrally on manubrium and ventrally on dens. Antennae 0.85 as long as (head + body) length, Ant. III and IV annulated. Ant. segment ratio as Ia:Ib:II:III:IV = 0.12:0.5:1:1.25:3.1. Tita of leg III longer than those of legs I and II; length 0.42, 0.48, 0.60 mm for Tita I, II, III. Tita with thin acuminate, smooth tenent hair, large number of serrated mes, few serrated mac and the ventro-distal smooth mes of Tita III. Labial triangle with 9–12 chaetae, at least one serrated and others smooth and no scales. Dorsal macrochaetotaxy as (3+4),(3+3)/0,2,3,(4+2+3+2). Unguis very slender and elongated with external edge basally sinuous, with one inner pair of equal basal teeth at 15 % from its base and one inner unpaired tooth at 40% from its base; unguiculus slender and pointed with small outer tooth at 30% from its base. Manubrium dorsally only with serrated mes, 2+2 ventro-apical serrated mes; dens with one short internal basal spine, mucro bidentate with one basal spine.

Description. Head and body length combined without antennae: 2.2mm. Abd. IV about 2 times as long as Abd. III. Color white, eyes absent, no pigment patch at their place.

Antennae. Antennae 0.85 as long as (head + body) length. Antennae 4,5 times longer than head diagonal. Ant. segment ratio as Ia:Ib:II:III:IV = 0.12:0.5:1:1.25:3.1. Ant. III and IV annulated, except the proximal part of Ant. III and the distal part of Ant. IV. Scales rounded, of medium size, their surface covered with numerous short spicules arranged longitudinally; numerous dorsally on Ant. Ib and II, absent on Ant. Ia, III and IV.

Ant. III–IV chaetotaxy with tendency to form whorls of chaetae, sometimes spiraling, without clear serial pattern across successive whorls. AIIIO located dorso-externo-apically, with 2 swollen S-chaetae side by side, surrounded internally by 1 thin short S-chaeta and externally by 1 pointed and bent, and 1 thin S-chaetae. Ant. IV with several thick subcylindrical S-chaetae in distal part, long, thick bifurcate subapical organite and subapical papilla devoid of "pin seta".

Mouthparts. Labral formula 4/5,5,4. No labral papillae. Prelabral and labral chaetae smooth, acuminate, of similar size. Labrum margin with inverted medial U-form intrusion devoid of primary granules, the distal smooth area large. Ventro-distally on labrum two unequal combs with one apical row of about 10 and 15 teeth respectively, and a pair of sinuous rods. Labial triangle with 9-12 chaetae, at least one serrated and others smooth, and no scales ( Fig. 55 ); lateral area (submentum) with 5 smooth chaetae. Maxillary outer lobe with one basal chaeta, a simple maxillary palp, 3 sublobal hairs and one smaller chaeta. Mandible asymmetrical with 5 teeth on the right and 4 on the left.

Head and body. Scales on head and body rounded to oval-elongated, hyaline, overlapping, of various size with a regular and dense cover of short spicules arranged in more or less regular lines. Chaetae, scales and trichobothria of the dorsal side of head and body are usually detached in microscopic preparations or on skins retrieved after DNA extraction.

Head dorsally with macrochaetae arranged as in Fig. 52 , and a dense cover of small scales and short serrated mes; laterally with scales mixed with medium size serrated mes; ventrally with smooth and serrated mes and no scales; 1+1 trichobothria posterior to ocular area.

Dorsal chaetotaxy illustrated in Fig. 52 . Pseudopore formula 1,1/1,1,1,1. Trichobothrial formula 1/0,0/0,2,3,2. Macrochaeta formula (3+4),(3+3)/0,2,3,(4+2+3+2). Th. II with 3 anterior and a line of 4 posterior mac; Th. III with 3 posterior and 3 lateral mac; Abd. IV with 4 medial, 1 or 2 posteromedial, 3 antero-lateral and 2 postero-lateral mac ( Fig. 52 ). S-chaetae arrangement not observable.

Ventral tube with smooth and serrated, pointed mes and mac, scales not observed. Overall chaetae number posteriorly and anteriorly not possible to observe. Each latero-distal flap with about 30 chaetae, most smooth pointed mes and several serrated mes. Genital plate of adult male consisting of numerous smooth mes, overall number not observable. Genital plate of subadult female with 2+2 mic.

Legs. Unguis very slender and elongated with external edge basally sinuous, with one inner pair of equal basal teeth at 15 % from its base and one inner unpaired tooth at 40% from its base ( Fig. 58 ). Small hyaline lamella covers claw, and bears 1+1 small latero-basal teeth ( Fig. 58 ). Unguis (internal edge): unguiculus = 1.2:1. Unguiculus slender and pointed with small outer tooth at 30% from its base ( Fig. 58 ).

Pretarsus with 1+1 minute mic.

Tibiotarsus with large number of serrated mes, thin tenent hair, large sockets probably of serrated mac (one observed in place on Tita II) and ventro-distal smooth mes of Tita III. Distal whorl of Tita with 10–12 serrated chaetae including thin, smooth acuminate tenent hair. Tita of leg III longer than those of legs I and II; length 0.42, 0.48, 0.60 mm for Tita I, II, III.

Femur with many serrated mes (some almost as large as serrated mac), smooth mac and scales. Ventrally at least 1, 1, 1 smooth macrochaetae on femora I, II, III. Biggest smooth mac as long as 0.32–0.4 the length of femur.

Trochanter with many chaetae ranging in size from mes to mac including many serrated mes, 1–2 smooth mac, and few smooth mes. Trochanteral organ of leg III with around 60 smooth mes. Scales not observed on trochanter I, present in small number on trochanter II and more numerous on trochanter III.

Chaetotaxy of coxa and subcoxa not observable.

Furca. Furca with pseudopores, different kinds of serrated mes and scales of various morphologies. Pseudopores present dorsally on each side of manubrium among distal group of chaetae, their overall number difficult to estimate. Manubrium dorsally with serrated mes and no scales; ventrally with medium size scales, without chaetae, except 2+2 apical serrated mes near axis. Ventro-basal part of manubrium not observable. Distal manubrial thickening with 5 to 7 small teeth on each side.

Dens not articulated, but constituted of short basal part hardly annulated, long medial part annulated dorsally and short, thinner, non annulated distal part about 4 times as long as mucro; covered by serrated chaetae and scales. Ventrally dense cover of medium size elongated scales, small and rounded on basal part of dens, increasing in size laterally to large, fusiform, pointed apically; scales absent in distal non-annulated part. One short and thick internal spine basally on each dens. Ratio manubrium: dens: mucro = 11,2: 20: 0.5. Mucro bidentate with one basal spine ( Fig. 60). Tenaculum with 4 teeth on each ramus and one chaeta socket (chaeta fallen on all specimens).

Discussion. The characters on which the Verhoeffiella specimens of Forat del Rastre have been identified as H. (V.) absoloni by Gama (1984) are not specified by the author. However, given that Gama did not examine the type material of the species, she must have relied on antenna length and inner tooth position on claw, which are the only features mentioned, but not illustrated, in the original and sole description of the species by Kseneman (1938). Gama (1984) characterized the Forat del Rastre specimens of H. (V.) absoloni , by four features: 1) antennae long but shorter than body; 2) claw elongated, with a pair of inner proximal teeth and an uneven unpaired inner tooth at 50% of its inner edge; 3) unguiculus long with a small outer tooth; 4) mucro curved, with apical tooth larger than the ante-apical one, with a thin basal chaeta. In addition, the author figured the pattern of dorsal macrochaetotaxy and the claw. Based on our own observation and Gama characterization of specimens from Forat del Rastre together with molecular comparison of specimens from the type locality in Montenegro and from the Catalan population we established that the population from Forat del Rastre is a new species described here as Heteromurus (Verhoeffiella) gamae sp. nov.

The discriminant characters between the different species of the subgenus Verhoeffiella , summarized in Tab. 3 , rely on a few characters usually considered as adaptive, and most published descriptions, except those of Gama (1984), lack information on modern taxonomic characters. Labrum, labial palp and mouthparts have not been described by authors. Dorsal macrochaetotaxy is available for 5 species. Most characters used in the redescription of H. (Verhoeffiella) absoloni and in the description of H. (V.) gamae sp. nov. given here are unknown in other species of the subgenus and therefore not included in the Tab. 3 . Considering the very basic available descriptions and the reference descriptive framework given here, all species of the subgenus need to be redescribed.

observations for H. (V.) absoloni . Most new characters used in the redescription of H. (V.) absoloni are not given in the

table as they are unknown in other species. Antennal segment ratio: values between brackets when given together for

(Ant Ia +Ib) or for fused segments. Asterisk (*) links the data in cells to source reference. medius Loksa & 1.6–2.1 shorter than body 0.13:0.5:1:1.75:2.63 (3+4),(≥1+3)/ Bogojević 1967 0,2,≥1,(3+0+≥ 2+≥2)

……continued on the next page Character Pair of basal teeth on unguis Inner unpaired Outer tooth on Unguis: Manubrium: tooth on unguis unguiculus unguiculus ratio (mucro+dens) ratio

absoloni big basal teeth big, at 50% from its present

(original description) base

Figures

FIGURES 50 – 53. Semi-diagrammatic macrochaetotaxy: 50, Heteromurus (Heteromurus) nitidus from Golubina pećina; 51, Heteromurus (Verhoeffiella) “ absoloni ” from Forat del Rastre as given by Gama (1984); 52, Heteromurus (Verhoeffiella) gamae sp. nov., our observation, pm-posteromedial mac; 53, Heteromurus (Verhoeffiella) absoloni, type population.

FIGURES 54 – 59. Heteromurus (Heteromurus) nitidus from Golubina pećina (54, 57), Heteromurus (Verhoeffiella) gamae sp. nov. (55, 58), Heteromurus (Verhoeffiella) absoloni from type locality (56, 59): 54 – 56, labial triangle chaetotaxy; 57 – 59, claw of leg III. Scales: 20 µm.

Tables

TABLE 3. Differential characters between species of the subgenus Verhoeffiella after the literature, with our own

absoloni (original description)	Source Kseneman 1938	Body length (mm)	Antenna: body ratio shorter than body	Antennal segment ratio	Antenna: head diagonal ratio	Abd. III:IV ratio	Dorsal macrochaeta formula
absoloni (redescription)	our observation	2.7–3.2	Ant. body+head = 0.54-0.68:1	0.15:0.61:1:1.5:2.0	3	1: 1.5	(3+4),(3+3)/ 0,2,3,(3+0+4+4)
anagastumensis	Lučić et al. 2008	4.35	Ant. body = 1.34:1	(0.7):1:2.64:3.67	5
cavicola	Absolon 1900*, Nosek & Paoletti 1985**	3.5–4.32		0.2:0.7:1:1.55:2.65		1: 2
constantius	Lučić et al. 2007	3.98	equal to body	0.13:0.53:1:2.13:2.47	4.7
constantinellus	Lučić et al. 2007	5.06	shorter than body	(0.21):1:(3.62)	2.4
dallaii	Nosek & Paoletti 1985	2.5–3.0	shorter than body	0.23:0.67:1:1.27:2.77	2.5	1: 2.8-3.0
gamae sp. nov.	our observation	2.2	Ant. body+head = 0.85:1	0.12:0.5:1:1.25:3.1	4,5	1: 2	(3+4),(3+3)/ 0,2,3,(4+2+3+2)
hispanica	Bonet 1931***, Gama 1984****, Nosek & Paoletti 1985	4	shorter than body	(0.8):1:2.3:2.4	4.3	1: 1.5	(?+4),(≥1+3)/ 0,3,3,(3+0+?+?)
longicornis	Absolon 1900*, Kseneman 1938, Nosek & Paoletti 1985**	5.3	Ant. III-IV longer than body	0.12:0.67:1:(7.76)		1: 1.5
cf. longicornis (Spanish records)	Gama 1984		Ant III-IV not longer than body				(?+3),(≥1+2)/ 0,1,0,(1+0+?+?)