Prionospio banyulensis Laubier, 1966

Hektoen, Martin M., Radashevsky, Vasily I. & Bakken, Torkild, 2025, Partial revision of northern European Prionospio Malmgren, 1867 (Annelida: Spionidae), European Journal of Taxonomy 1027, pp. 1-58 : 5-10

Prionospio banyulensis Laubier, 1966

Figs 2–3

Prionospio banyulensis Laubier, 1966: 258 .

Prionospio ockelmanni Pleijel, 1985: 177–181 , figs 1–3.

Prionospio banyulensis – Laubier 1968: 99–105, figs 10–15. — Sigvaldadóttir 1992: 210–217, figs 1–5, table 1. — Kirkegaard 1996: 79, fig. 35. — Hektoen et al. 2024: figs 1, 4.

Prionospio ( Minuspio) banyulensis – Hartmann-Schröder 1996: 328–329.

Aurospio banyulensis – Sigvaldadóttir 1998: 186. — Sigvaldadóttir 2002: 210.

Diagnosis

Prostomium anteriorly rounded, posteriorly extending to end of chaetiger 1 as a short, thick caruncle. Median eyes large, crescentic. Three pairs of apinnate branchiae on chaetigers 3–5 similar in size to notopodial postchaetal lamellae. Neuropodial lamellae of chaetiger 2 quadrangular, upwards-turned, of chaetiger 3 subrectangular, upwards-turned. Sabre chaetae in neuropodia from chaetiger 10. Hooded hooks in neuropodia from chaetigers 11–14.

Type material of Prionospio banyulensis

Neotype

FRANCE • Banyuls-sur-Mer , Cap d’Osne; 42°29.8′ N, 3°8.48′ E; depth 24 m; 9. Oct. 1991; stn Banyuls 1991h; van Veen grab; designated by Sigvaldadóttir (1992); SMNH Type-4422.

Type material of Prionospio ockelmanni

Holotype

SWEDEN • Öresund ; depth 29 m; 11 Sep. 1976; Fredrik Pleijel leg.; stn Öresund 1976; SMNH Type- 3358.

Paratypes

SWEDEN • 3 specs; Öresund ; depth 29 m; 11 Sep. 1976; Fredrik Pleijel leg.; stn Öresund 1976; SMNH Type-3358 .

Other material examined

FRANCE • 1 spec.; Banyuls-sur-Mer , Coralligene; 42°30.220′ N, 3°8.300′ E; depth 18 m; 14 Jan. 1991; stn Banyuls 1991f; van Veen grab; SMNH 111890 • 1 spec.; Banyuls-sur-Mer; Arne Nygren leg.; stn 257; NTNU-VM 84125 • 3 specs; Banyuls-sur-Mer ; Fredrik Pleijel leg.; 1 Oct. 1993; LACM-AHF Poly 4424 .

NORWAY – Møre og Romsdal • 1 spec.; Smøla, Andholman; 63°28.017′ N, 7°51.455′ E; depth 22 m; 17 Dec. 2019; Åkerblå AS leg.; stn AND-7; van Veen grab; NTNU-VM 84030 . – Trøndelag • 1 spec.; Hitra Singsholmen; 63°24.876′ N, 8°25.368′ E; depth 41 m; 18 Nov. 2020; Åkerblå AS leg.; stn SIN-2; van Veen grab; SEM stub; NTNU-VM 84148 • 1 spec.; same data as for preceding; NTNU-VM 84035 • 1 spec.; Frøya, Olaugsskjaeret; 63°47.664′ N, 8°31.230′ E; depth 36 m; 6 Nov. 2019; Åkerblå AS leg.; stn OLA-1; van Veen grab; NTNU-VM 84026 • 4 specs; Bjugn Havsund; 63°48.073′ N, 9°26.799′ E; depth 22 m; 27 Aug. 2019; Åkerblå AS leg.; stn HAV-3; van Veen grab; NTNU-VM 84024 • 1 spec.; Frøya, Tennøya; 63°48.327′ N, 8°27.493′ E; depth 120 m; 13 Aug. 2020; Åkerblå AS leg.; stn TEN-4; van Veen grab; SEM stub; NTNU-VM 84147 • 7 specs; Steinskjaer Tjuin; 64°4.367′ N, 11°14.203′ E; depth 25 m; 16 Jul. 2020; Åkerblå AS leg.; stn TJU-3; van Veen grab; NTNU-VM 84036 • 1 spec.; same data as for preceding; SEM stub; NTNU-VM 84149 • 1 spec.; Frøya, Kya ; 63°46.216′ N, 8°19.535′ E; depth 41 m; 27 Jul. 2022; stn Kya-5; van Veen grab; NTNU-VM 84142 . – Nordland • 3 specs; Herøy, Nordgåsvaer; 66°4.639′ N, 12°4.353′ E; depth 75 m; 27 Sep. 2021; Åkerblå AS leg.; stn NGÅ-2; van Veen grab; NTNU-VM 84031 . – Troms • 5 specs; Tranøy, Hallvarsøya; 69°9.284′ N, 16°54.531′ E; depth 60 m; 29 Oct. 2019; Åkerblå AS leg.; stn HAL-4; van Veen grab; NTNU-VM 84023 • 1 spec.; Senja, Ørnfjordbotn; 69°29.640′ N, 17°39.969′ E; depth 80 m; 14 Jul. 2021; Åkerblå AS leg.; stn ØRN-3; van Veen grab; NTNU-VM 84025 • 1 spec.; Karlsøy, Korsnes; 69°59.065′ N, 19°55.377′ E; depth 101 m; 18 Sep. 2019; Åkerblå AS leg.; stn KOR-1; van Veen grab; SEM stub; NTNU-VM 84150 • 1 spec.; same data as for preceding; SEM stub; NTNU-VM 84151 • 2 specs; Karlsøy, Karanes; 70°4.132′ N, 19°18.715′ E; depth 73 m; 11 Aug. 2021; Åkerblå AS leg.; stn KAR-4; van Veen grab; NTNU-VM 84068 • 1 spec.; Karlsøy, Mjønes; 70°6.477′ N, 19°35.958′ E; depth 216 m; 7 Dec. 2021; Åkerblå AS leg.; stn MJØ-3; van Veen grab; NTNU-VM 84072 • 4 specs; Tromsø, Nordnibba; 70°9.855′ N, 19°21.322′ E; depth 73 m; 11 Oct. 2021; Åkerblå AS leg.; stn NOR-REF; van Veen grab; NTNU-VM 84034 • 2 specs; Tromsø, Nordnibba; 70°9.993′ N, 19°22.469′ E; depth 67 m; 11 Oct. 2021; Åkerblå AS leg.; stn NOR- 5; van Veen grab; NTNU-VM 84033 . – Finnmark • 2 specs; Alta, Langnes; 70°6.537′ N, 23°0.061′ E; depth 26 m; 22 Jun. 2022; Åkerblå AS leg.; stn LAN-1; van Veen grab; NTNU-VM 84066 • 11 specs; Hammerfest, Bårdfjord; 70°25.701′ N, 22°51.086′ E; depth 61 m; 3 Nov. 2021; Åkerblå AS leg.; stn BÅR-REF; van Veen grab; NTNU-VM 84032 .

SWEDEN – Halland • 1 spec.; Varberg, Värö ; 57°10.000′ N, 12°5.000′ E; depth 20 m; 1980; stn Varö spring 1980 2; van Veen grab; SMNH 9556 . – Bohuslän • 2 specs; Stora Fjädern; depth 35 m; stn St. Fjädern ; SMNH 111891 • 1 spec.; Väderöarna , SE of Hamnerö; depth 22–30 m; 10 Jul 1984; SMNH 111892 • 1 spec.; Kostergrund ; depth 40 m; 29 Jun 1990; stn Koster 1991; SMNH 111894 .

UNITED KINGDOM • 5 specs; Plymouth, Stoke point, Millbay channel; depth 35–40 m; 6 Jun. 1986; stn Ply 1986i; SMNH 111878 .

Examined material with sequence data

FRANCE • 1 spec.; Banyuls sur Mer ; leg. Arne Nygren leg.; stn 256; NTNU-VM 84037 .

NORWAY – Viken • 1 spec.; Drøbak; 59°38.694′ N, 10°36.702′ E; depth 125–130 m; 22 Oct. 2014; POLYSKAG exped.; stn POLYSKAG-2014/10-19; dredge; ZMBN 152614 . — Finnmark • 1 spec.; Hammerfest Borvika; 70°44.517′ N, 23°25.965′ E; depth 49 m; 26 Aug. 2020; Åkerblå AS leg.; stn BOR-REF; van Veen grab; NTNU-VM 84027 • 1 spec.; same data as for preceding; NTNU-VM 84028

• 1 spec.; Hammerfest, Borvika; 70°45.454′ N, 23°26.833′ E; depth 46 m; 26 Aug. 2020; Åkerblå AS leg.; stn BOR-2; van Veen grab; NTNU-VM 84029 .

Description (adults)

Neotype ( SMNH Type-4422) complete, 7 mm long, 0.15 mm wide, with 47 chaetigers, laterally flattened, likely due to previously being mounted on slide. Other complete specimens up to 12.6 mm long, 0.4 mm wide, with up to 65 chaetigers. Color in alcohol pale white. Prostomium anteriorly broadly rounded, posteriorly extending to end of chaetiger 1 as a thick caruncle ( Fig. 2A). Nuchal organs U-shaped ciliary bands lateral to caruncle. Two pairs of eyes arranged trapezoidally, bright red in alcohol, red to dark brown in formalin, color fading during storage in alcohol. Median eyes large, crescent- to oval-shaped; lateral eyes large round spots, situated anteriorly and set wider apart. Dorsolateral parts of peristomium fused with notopodial postchaetal lamellae of chaetiger 1, forming ear-shaped structures lateral to prostomium ( Fig. 2A). Palps missing in neotype, in other specimens as long as 10–15 chaetigers.

Branchiae on chaetigers 3–5, apinnate, with dense ciliation on lateral edges, approximately equal in size, slightly longer than notopodial postchaetal lamellae ( Fig. 2A, 3A). Nototrochs transverse ciliary bands on chaetiger 2 and between bases of branchiae of chaetigers 3 and 4. Dorsolateral longitudinal ciliation absent.

Notopodial prechaetal lamellae small, rounded on chaetigers 2 and 3, inconspicuous on succeeding chaetigers. Notopodial postchaetal lamellae of chaetiger 1 fused with dorsal posterior parts of peristomium; lamellae subrectangular on chaetiger 2, largest on chaetigers 3 and 4, sometimes with short tips on branchiate chaetigers ( Figs 2A, C–D), smaller on postbranchiate chaetigers ( Figs 2A, 3A), oval from chaetigers 7–8 onwards. Low dorsal crests present between notopodial lamellae from chaetigers 6–9 to chaetigers 10–15 ( Figs 2A, 3A). Neuropodial prechaetal lamellae inconspicuous. Neuropodial postchaetal lamellae of chaetiger 1 small and oblong, of chaetiger 2 subtriangular, higher than long and slightly upwards-pointed ( Fig. 2C), of chaetiger 3 triangular with upwards-pointed tip ( Fig. 2D), rounded, small from chaetiger 4 onwards ( Fig. 2E–F). Interneuropodial pouches absent.

Notopodial capillaries on anterior chaetigers arranged in two rows, unilimbate and slightly granulated. Anterior row shorter than posterior row. Notopodial capillaries in middle and posterior chaetigers alimbate, long, thin, sometimes coiled. Neuropodial capillaries arranged in two rows on anterior chaetigers unilimbate, granulated, anterior row shorter than posterior row. Sabre chaetae in neuropodia from chaetiger 10, with slight granulation on distal part, one or rarely two per fascicle ( Fig. 2B). Hooded hooks in notopodia from chaetigers 23–43; in neuropodia from chaetigers 12–14, up to nine in a series, alternating with 1–3 capillary chaetae. Both noto- and neuropodial hooks with 4–5 pairs of upper teeth arranged in two vertical rows above main fang, with outer and inner hoods.

Pygidium with one long middorsal cirrus and one pair of short ventral cirri.

Reproduction

Prionospio banyulensis is dioecious. Of the 12 sexually mature individuals studied, seven were males and five were females. The smallest mature worms had about 45 chaetigers. In both females and males, gametes develop from chaetiger 10 to chaetigers 33–60. Spermatids were interconnected in tetrads; spermatozoa were ect-aquasperm with spherical nucleus about 2 µm in diameter. Largest oocytes were about 70 µm in diameter, with smooth envelope about 2 µm thick having single depression about 10 µm in diameter and 5-6 µm deep; nucleus was about 27 µm in diameter, with a single nucleolus about 8 µm in diameter. The mature individuals had notopodial capillaries essentially longer than capillaries in juveniles, indicating possible swimming and swarming during spawning event.

Remarks

Prionospio banyulensis was originally described from Banyuls-sur-Mer, Mediterranean Sea, France. Laubier (1966) first provided brief notes about the ecology of P. banyulensis and then described the morphology of this species ( Laubier 1968) but never designated type specimens. Sigvaldadóttir (1992) redescribed P. banyulensis , designated a neotype, and for the first time reported the species from northern Europe. Moreover, Sigvaldadóttir (1992) treated Prionospio ockelmanni Pleijel, 1985 , described from Öresund, Sweden, as a junior synonym of P. banyulensis . Based on the results of a phylogenetic analysis of morphological characters of the species of the Prionospio- complex, where P. banyulensis formed a monophyletic group with Aurospio dibranchiata, Sigvaldadóttir (1998) transferred P. banyulensis to Aurospio . Blake et al. (2020: 59) noted that some species of Prionospio have erroneously been assigned to Aurospio “based almost entirely on the first occurrence of branchiae from chaetiger 3 instead of chaetiger 2”. They proposed that several species listed among Aurospio should be referred to Prionospio but did not act at that time. Hektoen et al. (2024) moved banyulensis back to Prionospio according to the results of a phylogenetic analysis of molecular data and noted that the remaining species of Aurospio should be further studied. Our re-examination of the types of P. banyulensis and P. ockelmanni supports their conspecificity. The neotype of P. banyulensis is not imaged here as camera-equipped microscopes were not available at SMNH.

Sigvaldadóttir (1992) found specimens of P. banyulensis with two and three pairs of branchiae from chaetiger 3. We examined a greater number of specimens than in previous studies, some of larger sizes than previously reported. We found specimens with a greater variation in branchial configuration that potentially belongs to P. banyulensis . In addition to dibranchiate (two pairs) and tribranchiate (three pairs) specimens, worms with four ( Fig. 3B, D) and five pairs of branchiae occurred. All worms with more than three pairs of branchiae were found from Norwegian coastal waters, while specimens with two and three pairs of branchiae occurred in both Norway and the type locality of Banyuls. No other differences in morphological characters were apparent, and the specimens with 4 and 5 pairs of branchiae were always found together with P. banyulensis with three pairs of branchiae, and were generally larger in size, indicating the number of branchiae could be a size related character. In dibranchiate specimens, the branchiae were present on chaetigers 3 and 4, while tribranchiate specimens had branchiae on chaetigers 3–5. Specimens with four pairs of branchiae had them on chaetigers 2–5 (NTNU-VM 84023, 94142), and specimens with five pairs had branchiae on chaetigers 2–6 (NTNU-VM 84024). However, there were two exceptions: one specimen had three pairs of branchiae starting from chaetiger 2 (NTNU-VM 84150; Fig. 3C), and another had four pairs starting from chaetiger 3 (NTNU-VM 84147; Fig. 3B).

All specimens of P. banyulensis sequenced by Hektoen et al. (2024) were studied here. This material was collected from Banyuls, the Oslofjord, and Finnmark. The individual from the type locality (NTNU-VM 84037) had two pairs of branchiae, while the remaining worms (ZMBN 152614, NTNU-VM 84027- 84029) had three pairs of branchiae. This molecular evidence supports a single, widely distributed species with some intraspecific variation in branchial number. However, Hektoen et al. (2024) did not include any specimens with more than three pairs of branchiae in their analysis, and only six such specimens were found in total. Thus, we cannot yet determine whether this broader variation represents intraspecific variation. At present, we treat all observed forms as P. banyulensis sensu lato, but the conspecificity of specimens with more than three pairs of branchiae must be confirmed by integrative taxonomic approaches.

Habitats and distribution

Mediterranean France, South England, Iceland, and along Swedish West and Norwegian coasts north to the Barents Sea. Found at depths of 18–216 m, mainly in coarse sand and shell hash.