Navarriella elliptica (Paladilhe, 1874)

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 202, pp. 1-17 : 10-13

Navarriella elliptica (Paladilhe, 1874) comb. nov.

( Figs 6–7 ; Supporting Information, Tables S4–S6)

Synonyms

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. Syntype PA/7, Bou/1, SMF 141895.

Lithabitella elliptica ( Paladilhe, 1874) – Boeters 1974: 90, figs 5–7. Topotype: BOE 358 ‘Mas Pascoulin in Serres 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: ‘Santa Agueda area, Arriola, spring about 250m from the houses at brook’. Holotype MNCN 15.05/60162H, paratypes MNCN 15.05/60162P.

Type material: Syntypes PA/7, Bou/1, SMF 141895 .

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

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

Description

Shell cylindrical, whorls 4–5, height 1.6–2.1 mm, width 1.1–1.4 mm ( Fig. 6A–N ; Supporting Information, Table S4); periostracum whitish; protoconch of 1.5 whorls, c. 350 µm wide and nucleus c. 200 µm wide ( Fig. 6Q, R ); protoconch microsculpture pitted ( Fig. 6 S–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 attachment oval, located near the nucleus ( Fig. 6O, P ).

Radula taenioglossate with a central tooth formula 5–C–5/2– 2, basal-tonguebroadly‘V’shaped, cutting-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, Spain (FW2708).

Some 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 (Supporting Information, Table S5), positioned opposite approximate middle of ctenidium. Stomach almost as long as wide with two chambers almost equal in size, style sac slightly longer than wide ( Fig. 7F ; Supporting Information, Table S5). Nervous system scarcely pigmented, moderately concentrated (mean RPG ratio = 0.40; Supporting Information, Table S5); 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 ; Supporting Information, Table S6); 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; Sr1 pyriform with a long duct, placed just above the junction with the bursal duct; Sr2 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 ; Supporting Information, Table S6). Penis unpigmented, strap-like, distal end of the penis gradually tapering and attached 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 µS/cm, except in the type locality of Ascain (932 µS/cm). Navarriella elliptica cohabits with other molluscs such as Pisidium spp. and Ancylus spp. It is also found alongside Potamopyrgus antipodarum (J.E. Gray, 1843) in Ascain and species of Bythinella Moquin-Tandon, 1856 in Bermeo and Arrantaza (Basque Country).

The 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 Sr2. 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 ; Supporting Information, Figs S1–S8, Tables S4–S6). The large Sr1 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, Sr1, and Sr2 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). The 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 ; Supporting Information, Table S6). The 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). The shells of A. (N.) elliptica and A. (N.) pellitica are nearly indistinguishable based on the PCA and DLA results ( Fig. 5A–C ). The TPS plot reveals two different morphotypes, one being wider and the other more cylindrical. However, this variation could be considered as intraspecific variation attributable 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 (Supporting Information, Table S4).

Figures

Figure 1. Distribution of the studied populations of Alzoniella (Navarriella) in the north of the Iberian Peninsula. Label abbreviations are explained in Supporting Information, Table S1. * indicates the sampled topotypes.

Figure 4. Statistical parsimony network based on COI haplotypes for the sampled populations of Alzoniella (Navarriella) elliptica and Alzoniella (Navarriella) pellitica. The circles are colour-coded by population and represent the number of haplotypes.Each vertical bar represents one mutation. The codes of the figure are explained in Supporting Information, Tables S1, S2. Asterisks indicate the sampled topotypes.

Figure 5. Geometric Morphometric analyses for the shells of Alzoniella (Navarriella) species based on 20 coordinates (eight landmarks and 12 semilandmarks).A, Principal Component Analysis (PCA) for species. B, Linear Discriminant Analysis (LDA) for species.C, PCA for populations. D, Thin-plate spline (TPS) plot displaying expansion (in red) and contraction (in blue) of the shell shape.Label abbreviations are explained in Supporting Information, Table S1.

Figure 6. Intraspecific variation of the shell shape, protoconch and opercula of Navarriella elliptica. A–N, shells.O–P, operculum. Q–V, protoconch and details of protoconch. A, I, K, M, T, and U, FW2611—spring in Arrarats, Navarra, Spain. B, N, O, P, and R, FW2623—spring next to Araxes River, Navarra, Spain. C, FW2708—watercourse from Roncesvalles to Valcarlos, Navarra, Spain. D and V, FW2712—spring in Chemin d’Andienea, Ascain, France. E, FW2717—spring in Arriola, Navarra, Spain. F, FW2591—spring in Arronategi Auz, Vizcaya, Spain.G, FW2594—spring in Nuarbe Auzoa, Guipúzcoa, Spain. H, spring in Ola, Navarra, Spain. J and L, FW2615—spring in Arrantza, Navarra, Spain. Q and S, FW2592—spring near Mañu Auzoa, Bermeo, Vizcaya, Spain.

Figure 7. Radulae and anatomy of Navarriella elliptica. A, central radular teeth; B, lateral and central radular teeth; C, inner marginal teeth; D, outer marginal teeth; E, ctenidium and osphradium; F, stomach; G, perioesophageal nervous ring; H, J, female genitalia; K, prostate gland; L, M, penis relaxed; N–Q, penis contracted.A–D, FW2708—watercourse from Roncesvalles to Valcarlos, Navarra, Spain. E–I, K–M, FW2591— spring in Arronategi Auz, Vizcaya, Spain. J, FW2717—spring in Arriola, Navarra, Spain. N–Q, FW2623—spring next to Araxes River, Navarra, Spain.Ag, albumen gland; Bc, bursa copulatrix; Cg, capsule gland; Sr1, distal seminal receptacle; Sr2, proximal seminal receptacle; P, penis; Pl, penis lobes.

Figure3.Phylogenetic relationships ofhydrobiid taxa incorporating thespecies of Alzoniella(Navarriella).A,Bayesian tree ofthe family Hydrobiidae basedon theconcatenated dataset (COI and 18S), including some selected species ofthe hydrobiidsubfamilies (highlighted with vertical bars). Brancheswith bootstrap support (BS) values fromthe maximumlikelihood (ML) analysis and Bayesian posterior probabilities(BPP) greater than 75% and 0.95,respectively,are indicatedwith asterisks.Branches only with BS> 75% are denoted with a triangle.Branchesonly with BPP> 0.95are shownwith a square.B, Bayesian phylogenetictree ofspecimens of Alzoniella (Navarriella) based onthe concatenated dataset(COI, 16S, H3, and 28S).BS and BPP areprovided abovebranches when greaterthan 75% and 0.95,respectively.The first vertical bar representsthe taxonomic species of eachpopulationassigned in previous studies asAlzoniella (Navarriella) elliptica (in red)and Alzoniella (Navarriella) pellitica (in blue).The remaining vertical barsrefer to thespecies delimitation methods:ABGD,distance-based automatic gap discovery;GMYC, single-thresholdgeneralized mixed Yule-coalescent;bPTP, Bayesian approach ofthe Poisson Tree Processes;mPTP,multirate PoissonTree Processes.ThebPTP bar is displayed with its Bayesian support value.Labelabbreviations areexplained in Supporting Information,Table S2. Scale bars:expected change per site.