Prionospio from the coast of the Iberian Peninsula, with the description of two new species (Annelida, Spionidae)

Abstract Five species of Prionospio Malmgren, 1867, each with four pairs of branchiae, are studied from coast of the Iberian Peninsula. Two of these species, Prionospiocristaventralissp. n. and P.paraparisp. n., are new to science, whereas P.caspersi Laubier, 1962, P.fallax Söderström, 1920, and P.ehlersi Fauvel, 1928 have been previously recorded. Prionospiocristaventralissp. n. is characterized by having ventral crests present on chaetigers XI–XIX, dorsal crests and low crests on chaetigers X–XXXIV, triangular neuropodial postchaetal lamellae with pointed ventral edges on chaetiger II, oval neuropodial lamellae on chaetiger III, digitiform pinnules on the posterior face of the first and fourth pairs, and branchial pairs II and III are triangular. Prionospioparaparisp. n. is characterized by having rounded neuropodial postchaetal lamellae on chaetiger I, digitiform pinnules on the posterior face of the first and fourth pairs, branchial pairs II and III are cirriform, low dorsal crests on chaetigers VIII–IX, and oval neuropodial lamellae with enlarged dorsal edges on chaetiger III. A key is given to all Prionospio species with four pairs of branchiae known from the Iberian Peninsula coastline.


Introduction
Prionospio was established by Malmgren (1867) for P. steenstrupi Malmgren, 1867, a spionid species with branchiae on chaetigers II-V, the first and fourth pairs of which are pinnate, and the second and third pairs apinnate. With the discovery of additional species, the diagnosis of the genus was widened to include species with different branchial shapes and arrangements, with the chaetiger upon which the branchiae first arise being particularly relevant. Variability has thus increased, making Prionospio a very heterogeneous genus with about 100 species (Sigvaldadóttir 1998). As a result, several authors have suggested that some of these should be reclassified into new genera and/or subgenera (Foster 1971, Blake and Kudenov 1978, Maciolek 1985, Wilson 1990, Sigvaldadóttir 1998. So far Prionospio caspersi Laubier, 1962, P. fallax Södreström, 1920, and P. ehlersi Fauvel, 1928 have been recorded from the Iberian Peninsula: the former from Catalonia (Desbruyères et al. 1972) and from off Aveiro (Ravara and Moreira 2013); the second from several localities on the Portuguese coast (Quintino and Gentil 1987;Quintino et al. 1989;Dexter 1992;Pardal et al. 1992;Gil andSardá 1999, Ravara andMoreira 2013) and the third from the Bay of Biscay (Aguirrezabalaga and Cebeiro 2005), from Coruña (Amoureux 1972, López Jamar andGonzález 1986), from off Aveiro and off Porto (Amoureux 1974, Pardal et al. 1992, and from the South western continental shelf of Portugal (Gil 2011). In this study, we examined material deposited in the Museo Nacional de Ciencias Naturales de Madrid previously identified as P. caspersi and P. fallax.
Following the careful comparison between the redescription of P. fallax by Sigvaldadóttir and Mackie (1993), redescription of P. ehlersi by Mackie and Hartley (1990) as well as the original description of P. caspersi, we describe two new species: P. cristaventralis sp. n. and P. parapari sp. n. An identification key and a map with type localities are provided for all known Prionospio species with four branchial pairs from the coastline of the Iberian Peninsula (Fig. 1).

Materials and methods
The material examined belongs to the collections maintained at the Museo Nacional de Ciencias Naturales de Madrid, Spain (MNCNM) and the Alcalá de Henares University, Spain, as well as the personal collection of J Parapar at the University of La Coruña, Spain. Type specimens of the two newly described species are deposited in the MNCNM. For each species, the location where the specimens were collected is indicated in their respective sections.
All material was fixed in 10% formaldehyde in sea water and preserved and stored in 70% ethanol. In order to examine some morphological characters, specimens were dipped first into water and then into methyl green solution for staining. The color fades quickly when specimens are returned to the alcohol solution (Warren et al. 1994). Specimens were measured with a millimeter ruler: body widths refer to the maximum postbranchial body width (including parapodia but not chaetae) at about chaetiger VIII. The eye color mentioned in the descriptions of the species was based on preserved organisms.
Remarks. The specimens examined in this study agree with the original and subsequent descriptions of the species (Laubier 1962, Imajima 1990, Dagli and Çinar 2009. However, there is a slight difference between our specimens and Dagli and Çinar's specimens: the sabre chaetae were reported as present from chaetiger X by Dagli and Çinar (2009) whereas they first appear on chaetiger XI in our specimens. There are a few further differences between the specimens examined here and the description given by Imajima (1990). Imajima (1990) described the prostomium as being broadly flared anteriorly, with a slight medial indentation and unilimbate chaetae, whereas the specimens in this study have a narrower prostomium that is slightly truncate to convex anteriorly, with bilimbate chaetae. Due, to these morphological differences, the identity of the specimens recorded as P. caspersi from Japan by Imajima (1990)  Description. Incomplete specimens, 3.0-11.0 mm long, with 13-40 chaetigers, 0.6-1.0 mm wide. Posterior fragment 9.0 mm long for 26 chaetigers, 0.8 mm wide. Color in alcohol pale white. Some specimens with oocytes on chaetigers XXX-XXXIV.
Four pairs of branchiae present on chaetigers II-V, first pair longest and thickest (Fig. 2D); sometimes first and fourth pairs equal in length or fourth pair slightly longer than first. First pair with long, dense digitiform pinnules on lateral and posterior faces, continuing to tip; central stem of branchial pair 1 pinnate, cylindrical, very thick and with a blunt tip ( Fig. 2A, D). Pairs 2-4 apinnate; pairs 2 and 3 triangular, thick (Fig. 2D, E), slightly expanded distally, with rounded tips, densely ciliated laterally, shorter than notopodial lamellae and pinnate pair. Pair 4 cirriform (Fig. 2D), basally united by a short, moderate dorsal cord-shape (Fig. 2D); branchiae subequal to, or longer than, notopodial lamellae; some specimens with regenerating branchiae.
Remarks. Prionospio cf. ehlersi is very similar to the original and subsequent descriptions of P. ehlersi (Fauvel 1928, Mackie andHartley 1990), in that both describe the same prostomial shape, branchial arrangement, and hooded hook structure, and all have interparapodial pouches. However, specimens of this study differ from P. ehlersi in that the former have oval (rather than triangular to subtriangular) notopodial lamellae on chaetiger I, the neuropodial lamellae on chaetigers IV-V are oval (rather than rounded), and the second and third branchial pairs are triangular and thick (rather than expanded or swollen distally), a dorsal cord-shape (rather than low crest) on chaetiger V is present, and the sabre chaetae in P. cf. ehlersi are alimbate (rather than sheathed). Mackie and Hartley (1990) reported a variation in the shape of chaetiger I notopodial postchaetal lamellae, and so considered this unimportant. They also noted some parapodial variation around chaetiger XVIII-XX. They did not mention the oval anterior neuropodial postchaetal lamellae, however, Fauvel (1928, fig. 1b) shows a chaetiger IV with neuropodial lamella very similar to that in this study (Fig. 2J). We consider that these differences are important, but we consider it premature to erect a new species with these specimens, without being able to first compare them with Fauvel's syntype material. The syntypes are deposited at the Museum National d'Histoire Naturelle, Paris under MNHN A438, A449. However, the material cannot be sent abroad for re-examination.
Remarks. These specimens match the redescription given by Sigvaldadóttir and Mackie (1993), except that we found some specimens with eyes and others without eyes; one specimen had a single large brown eyespot. Possibly, the variation is due to the preservation of the specimens.
Pygidium missing. Remarks. Prionospio cristaventralis sp n. is similar to P. multicristata Hutchings & Rainer, 1979, P. nirripa Wilson, 1990, P. nielseni Hylleberg & Nateewathana, 1991, P. cornuta Hylleberg & Nateewathana, 1991, and P. paradisea Imajima, 1990 in that all show the same prostomial shape and neuropodial postchaetal lamellae on chaetigers II-III. However, P. cristaventralis sp. n. differs from these species due to the presence of ventral crests and dorsal crests limited to chaetigers X-XI, and low dorsal crests on chaetigers XII-XXII/XXXIV (end fragment) compared to low dorsal crests from chaetigers VII to XXV-XXX in P. multicristata, low dorsal crests from X-XIII to XX-VIII-XXXVII in P. nirripa, P. nielseni and P. cornuta and high crests from X to LX in P. paradisea. Prionospio cristaventralis sp. n. is also similar to P. pacifica Zhou & Li, 2009 in that both species have dorsal and ventral crests or folds. However, P. cristaventralis sp. n. can be distinguished from P. pacifica by having a prostomium that is rounded anteriorly (instead of being truncate), dorsal crests on chaetigers IV-V (instead of lacking such crests), and ventral crests on chaetigers XI-XIX (instead of only on chaetiger IX). The presence of ventral crests appears to be a unique feature of these two species.
Four pairs of branchiae present on chaetigers II-V (Fig. 4B, C); first pair longer than fourth pair, up to 1 time and a half longer than the fourth pair. Pairs 1 and 4 with long, slender, dense digitiform pinnules arranged along posterior face of the stems, pinnules thick, long, blunt in middle region of branchiae (Fig. 3B); branchiae with very long, naked, smooth, distal tips (Fig. 4B). Pairs 2 and 3 apinnate, cirriform, long, densely ciliated laterally, with pointed tips (Fig. 4E, F); subequal in length, up to 3 times shorter than pinnate pairs, but longer than notopodial lamellae (Fig. 4B, E, F).
Pygidium with one long median cirrus and two short, lateral lobes (Fig. 4X).
Remarks. Prionospio parapari sp. n. is very similar to P. fallax in having a prostomium that is truncated on the anterior margin, a neuropodial postchaetal lamellae on chaetiger II being the same shape, and a high dorsal crest on chaetiger 7. However, P. parapari sp. n. can be distinguished from P. fallax as redescribed by Sigvaldadóttir and Mackie (1993), by the former having rounded (rather than rectangular) postchaetal neuropodial lamellae on chaetiger I, the first pair of branchiae longer than fourth (rather than of equal size), and with dense digitiform (rather than sparse lateral) pinnules arranged along the posterior face of the stems on branchiae 1 and 4, and cirriform (rather than subtriangular) second and third branchial pairs. In addition, the low dorsal crests in P. parapari sp. n. are present on chaetigers VIII-IX while in P. fallax they are absent; the neuropodium on chaetiger III in P. parapari sp. n. is oval with an enlarged dorsal edge whilst in P. fallax it is subtriangular and dorsally pointed; and the sabre chaetae in P. parapari sp. n. are heavily granulated and bilimbate whereas in P. fallax they are distally granulated and alimbate. The pygidium lacks pigmentation in P. parapari.
Prionospio parapari sp. n. is also similar to P. komaeti Hylleberg & Nateewathana, 1991, P. depauperata Imajima, 1990, and P. oligopinnulata Delgado-Blas, 2015, in that all three species have a prostomium that is truncated on the anterior margin, the same shaped neuropodial postchaetal lamellae on chaetiger II, and a high membranous dorsal crest on chaetiger VII that decreases in height on chaetigers VIII-IX. However, P. parapari sp. n. differs from the first two species in that it has rounded (rather than square or lanceolate) notopodial and neuropodial postchaetal lamellae on chaetiger I, and an oval neuropodium on chaetiger III with the dorsal edge enlarged (rather than one that is square or triangular). In addition, the branchiae of P. parapari sp. n. have long, naked, smooth distal tips, whereas those of P. komaeti and P. depauperata have pinnules extending to the distal end, and P. parapari lacks low dorsal crests on chaetigers X-XI/XIII. Prionospio parapari sp. n. also differs from P. depauperata in that it has sabre chaetae without a distal filament, the notopodial hooded hooks start on chaetigers XIX-XXXVIII rather than XLV-XLVII, and the pygidium has two long lateral lobes rather than two short lateral cirri. Furthermore, P. parapari sp. n. is similar to P. oligopinnulata in that both species show the same pygidial structure, but differs in having cirriform rather than triangular second and third branchial pairs. In addition, the low dorsal crests on chaetigers X-XIV are absent in P. parapari sp. n., the neuropodium on chaetiger III is oval with the dorsal edge enlarged (rather than subtriangular and ventrally pointed), and the sabre chaetae are bilimbate (rather than alimbate). Prionospio parapari sp. n. is similar to P. rotunda Delgado-Blas, 2015 in that both species have large, rounded neuropodial postchaetal lamellae on chaetiger I, cirriform second and third branchial pairs, the first branchial pair always longer than fourth pair, and the same pygidium structure. However, P. parapari sp. n. differs from P. rotunda in having a bottle-shaped prostomium that is truncated on the anterior margin (rather than a pyriform and rounded one). In addition, the low dorsal crests in P. parapari sp. n. are present on chaetigers VIII-IX whereas in P. rotunda they are absent, and the neuropodium on chaetiger III is oval with an enlarged dorsal edge (rather than rounded). The differences between this new species and the other species examined are provided in the key.
Etymology. The species is named in honor of Dr Julio Parapar, in recognition of his major contribution to the study of polychaetes from Spanish coasts.
Type locality. Ría de Ferrol and the mouth of Piedras River, Huelva, Spain. Distribution. To date, this species has been recorded only on the Spanish Atlantic coast (Ria de Ferrol and the mouth of Piedras River, Huelva).