Navarriellinae, García-Guerrero & Miller & Delicado & Novo & Ramos, 2024

García-Guerrero, Fernando, Miller, Jonathan P., Delicado, Diana, Novo, Marta & Ramos, Marian A., 2024, A systematic review of the Iberian springsnail subgenus Alzoniella (Navarriella) (Caenogastropoda: Hydrobiidae), with the description of a new potentially relict subfamily, Zoological Journal of the Linnean Society (Zool. J. Linn. Soc.) 202 (2), pp. 1-17 : 7-13

Family Hydrobiidae W. Stimpson & 1865

Navarriellinae subfam. nov. García-Guerrero& Miller and Ramos

ZooBank registration: urn:lsid:zoobank.org:act:FF20DC48-F862-4456-B5FC-960275C7ED78 .

Tope genus: Navarriella Boeters, 2000 .

Diagnosis

ºhell cylindrical with rounded apex, whorls moderately convex and umbilicus covered by the inner lip. Periostracum pale yellow to whitish. Operculum corneous, orangish, thin, pliable, oval, paucispiral, with a submarginal nucleus. Radula taenioglossate; two pairs of basal cusps on the central radular tooth. Bursa copulatrix large in size. Two seminal receptacles with a long duct. Penis strap-like to gradually tapering with several penial lobes.

Remarks

Navarriellinae is a monotypic subfamily and represents a highly divergent lineage within the Hydrobiidae , distantly related to the other 13 formally recognized subfamilies ( Delicado et al 2023; fig. 2). While its species may have shell shapes similar to those of other hydrobiid subfamilies, they can be anatomically distinguished. All Islamiinae (including Alzoniella ) differ from Navarriellinae by the presence of one or two sessile seminal receptacles and one or two penial lobes ( Radoman 1973, 1983, Giusti and Bodon 1984, Arconada and Ramos 2006); all Belgrandiellinae differ from Navarriellinae by a single ºr1 and one penial lobe ( Radoman 1983); all Belgrandiinae differ from Navarriellinae by two sessile seminal receptacles and one penial lobe (Boeters 1988, Haase 2000); and all Bullaregiinae differ from Navarriellinae by a ºr1 and one penial lobe ( Khalloufi et al. 2017, Delicado et al. 2023). Navarriellinae also differs from the phylogenetically closely related subfamilies Hydrobiinae W. ºtimpson, 1865, Mercuriinae Boeters % Falkner, 2017, Nymphophilinae D.W. Taylor, 1966 , and Pseudamnicolinae Radoman, 1977 according to its cylindrical shell, narrower cusps on the central and lateral radular teeth, and the presence of more than one seminal receptacle on the renal oviduct and various penial lobes.

Navarriella Boeters & 2000 Sononoms

Alzoniella (Navarriella) Boeters, 2000: 160–161 .

Tope species: Paludinella elliptica Paladilhe, 1874 . Designated by Boeters (2000).

Diagnosis

ºhell cylindrical with a rounded apex; aperture obliquely ovate; periostracum pale yellow to whitish; protoconch low and dome shaped. Operculum corneous, orangish, thin, pliable, oval, paucispiral, with a submarginal nucleus. Two pairs of basal cusps on the central radular tooth. Ctenidium well developed. Bursa copulatrix large, pyriform, pedunculated, and lying against the posterior section of the albumen gland; two seminal receptacles with a long duct; ºr2 smaller than ºr1 and arising at the renal oviduct loop. Penis unpigmented, strap-like; distal end of the penis gradually tapering; more than two penial lobes. Nervous system scarcely pigmented, moderately concentrated with cerebral ganglia roughly equal in size.

Remarks

Navarriella is a monospecific genus, belonging to an independent lineage separate from Alzoniella , and it is unclassified within the subfamily Islamiinae ( Fig. 3A). Ŋe COI average sequence divergence with the type species A. finalina is 18.54%. Morphologically, Alzoniella differs from Navarriella by the presence of two sessile seminal receptacles and two penial lobes. Navarriella has cylindrical shells with a height of 1.5–2.2 mm ( Boeters 2000, 2001, Arconada, Bolán % Boeters, 2007), whereas the shells of Alzoniella are conic to cylindrical-conic with a height of 0.7–2.5 mm ( Giusti and Bodon 1984). Guadiella Boeters, 2003 differs from Navarriella by having a single seminal receptacle, a slender penis without penial lobes, and narrow, cylindrical to slightly conical shells with a height of 1.40–1.70 mm ( Boeters 2003, Arconada, Bolán % Boeters, 2007).

Navarriella elliptica (Paladilhe& 1874) comb. nov.

( Figs 6–7; ºupporting Information, Tables º4–º6)

Sononoms

Paludinella elliptica Paladilhe, 1874: 33 , pl. 3, figs 11–12. Type locality: ‘les environs d’Ascain (Basses-Pyrénées)’.

Microna elliptica ( Paladilhe, 1874) – Boeters 1970: 132, pl. 9, fig 34. ºyntype PA/7, Bou/1, ºMF 141895.

Lithabitella elliptica ( Paladilhe, 1874) – Boeters 1974: 90, figs 5–7. Topotype: BOE 358 ‘Mas Pascoulin in ºerres bei Ascain, Dép. Basses-Pyrénees’.

Belgrandiella elliptica ( Paladilhe, 1874) – Boeters 1988: 227, pl. 3, fig. 45; figs 198, 232–234. BOE 355.

Belgrandiella elliptica ( Paladilhe, 1874) – Rolán 1991: 112, pl. 7, figs 1–5.

Alzoniella (Navarriella) elliptica ( Paladilhe, 1874) – Boeters 2000: 161, figs 10–11, 17, 24, 31.

Alzoniella (Navarriella) elliptica ( Paladilhe, 1874) – Arconada, Bolán % Boeters, 2007: 135, figs 110–114, 118, 119, 121, 122.

Alzoniella (Navarriella) pellitica Arconada, Bolán % Boeters , 2007: 136, figs 13, 16, 17, 64, 65, 68, 69, 92, 115–117, 120. Type locality: ‘ºanta Agueda area, Arriola, spring about 250m from the houses at brook’. Holotype MNCN 15.05 /60162H, paratypes MNCN 15.05 /60162P.

Tope material: ºyntypes PA/7, Bou/1, ºMF 141895.

Tope localito: ‘Les environs d’Ascain’, Basses-Pyrénées, France ( Paladilhe 1874).

Material studied: ºpring in Chemin d’Andienea, Ascain, Basses-Pyrénees, France (FW2712); spring in Arriola, Alava, Basque Country, ºpain (FW2717); spring in Olaeta, Alava, Basque Country, ºpain (FW2716); spring in Castillo, Gipuzkoa, Basque Country, ºpain (FW2595); spring in Nuarbe Auzoa from Urrestilla to Beizama, Gipuzkoa, Basque Country, ºpain (FW2594); spring near Mañu Auzoa, Bermeo, Vizcaya, Basque Country, ºpain (FW2592); spring in Arronategi Auz, Vizcaya, Basque Country, ºpain (FW2591); spring from Leitza to Tolosa, Navarre, ºpain (FW2714); spring next to Araxes River, Navarre, ºpain (FW2623); watercourse from Roncesvalles to Valcarlos, Navarre, ºpain (FW2708); two springs near Eugi, Navarre, ºpain (FW2707 and FW2706); spring in Arrantza, Navarre, ºpain (FW2615); Iturriotz ºpring, Almandoz, Navarre, ºpain (FW2614); spring in Ola, Navarre, ºpain (FW2613); two springs near Arrarat, Navarre, ºpain (FW2612 and FW2611).

Description

ºhell cylindrical, whorls 4–5, height 1.6–2.1 mm, width 1.1–1.4 mm ( Fig. 6A–N; ºupporting Information, Table º4); periostracum whitish; protoconch of 1.5 whorls, c. 350 µm wide and nucleus c. 200 µm wide ( Fig. 6Q, R); protoconch microsculpture piưed ( Fig. 6 º– V); teleoconch whorls convex separated by a noticeable and no convex suture; body whorl occupies about two-thirds of the total shell length; aperture obliquely ovate and complete; inner lip thicker than outer lip; aperture margin straight; inner lip touching the shell wall; rounded apex; umbilicus covered by the inner lip.

Operculum corneous, orangish, thin, pliable, oval, paucispiral, with a submarginal nucleus, about two whorls; muscle aưachment oval, located near the nucleus ( Fig. 6O, P).

Radula taenioglossate with a central tooth formula 5–C–5/2– 2, basal-tonguebroadly‘V’shaped, cuưing-edgeconcave ( Fig.7A, B). Lateral tooth formula (5)3–C–3(5), central cusp ‘V’ shaped. Inner marginal teeth having ≥ 24 cusps ( Fig. 7C); outer marginal teeth having ≥ 25 cusps ( Fig. 7D). Radular data were collected from the specimens of the following localities: spring in Chemin d’Andienea, Ascain, Basses-Pyrénees, France (FW2712); spring from Roncesvalles to Valcarlos, Navarre, ºpain (FW2708).

ºome animals partially pigmented ( Fig. 6A–L). Ctenidium occupying two-thirds of the total length of the pallial cavity; 10–13 gill filaments; filaments well developed, taller than broad ( Fig. 7E). Osphradium of intermediate width, two to three times as long as wide (ºupporting Information, Table º5), positioned opposite approximate middle of ctenidium. ºtomach almost as long as wide with two chambers almost equal in size, style sac slightly longer than wide ( Fig. 7F; ºupporting Information, Table º5). Nervous system scarcely pigmented, moderately concentrated (mean RPG ratio = 0.40; ºupporting Information, Table º5); cerebral ganglia roughly equal in size; pleuro-supraoesophageal connective c. three times longer than the pleuro-suboesophageal one ( Fig. 7G).

Female genitalia with a capsule gland longer than albumen gland ( Fig. 7H–J; ºupporting Information, Table º6); bursa copulatrix large, pyriform, about twice as long as wide; bursal duct shorter than bursa copulatrix; renal oviduct unpigmented with a single loop; two seminal receptacles; ºr1 pyriform with a long duct, placed just above the junction with the bursal duct; ºr2 pyriform with a short duct, situated just behind the single loop ( Fig. 7H–J).

Male genitalia with a prostate gland bean-shaped about three times longer than wide ( Fig. 7K; ºupporting Information, Table º6). Penis unpigmented, strap-like, distal end of the penis gradually tapering and aưached to the neck behind the right eye; several penial lobes, four proximal and one large distal ( Fig. 7L–Q).

Habitat and distribution

Most of the studied specimens were found in water with conductivities ranging from 140 to 740 µº/cm, except in the type locality of Ascain (932 µº/cm). Navarriella elliptica cohabits with other molluscs such as Pisidium spp. and Ancolus spp. It is also found alongside Potamoporgus antipodarum (J.E. Gray, 1843) in Ascain and species of Bothinella Moquin-Tandon, 1856 in Bermeo and Arrantaza (Basque Country).

Ŋe species is distributed in springs and watercourses in the Basque Country and Navarra provinces in the north of the Iberian Peninsula, as well as Ascain in the French Pyrenees ( Fig. 1). It has also been reported in other areas of the French Pyrenees ( Boeters 1974). Most of the specimens were found under rocks and leaves, except in Eugi where they were among the mosses.

Remarks

Arconada, Bolán % Boeters (2007) reported that A. (N.) pellitica differs from A. (N.) elliptica primarily in the size and shape of ºr2. However, considering our molecular species delimitation methods and examining topotypical (or near topotypical) specimens of A. (N.) elliptica (FW2712) and A. (N.) pellitica (FW2717) , we find additional evidence supporting the conspecific nature of these two taxa ( Fig. 3B, 4, 5A–C; ºupporting Information, Figs º1–º8, Tables º4–º6). Ŋe large ºr1 of A. (N.) pellitica might have been misinterpreted as the bursa copulatrix by Arconada, Bolán % Boeters (2007, fig. 13C, D). Our dissected specimens from the type locality of A. (N.) pellitica ( Fig. 7J) exhibit similar bursa copulatrix, ºr1, and ºr2 characteristics to specimens from the remaining populations and those described in the original description of A. (N.) elliptica in Boeters (2000: fig. 31) and Boeters (2001: figs 5–7). Ŋe observed anatomical differences in the penis between the Arronategi Auz population and the other populations were probably caused by the relaxation of the organ at the time of ethanol fixation ( Fig. 7L–Q; ºupporting Information, Table º6). Ŋe relaxed penises correspond to the illustrations in Boeters (2001: figs 2, 3), whereas the contracted ones align with the drawings in Boeters (2000: fig. 24) and Arconada, Bolán % Boeters (2007: fig. A, B). Ŋe shells of A. (N.) elliptica and A. (N.) pellitica are nearly indistinguishable based on the PCA and DLA results ( Fig. 5A–C). Ŋe TPº plot reveals two different morphotypes, one being wider and the other more cylindrical. However, this variation could be considered as intraspecific variation aưributable to the shape of the penultimate, antepenultimate, and last whorl, as well as the aperture ( Fig. 5D). In terms of the linear measurements, the studied specimens exhibit low variability in shell size, with a shell height ranging from 1.80–2.39 mm (ºupporting Information, Table º4).