First record of Paraprionospio coora Wilson , 1990 ( Polychaeta : Spionidae ) in the Atlantic Ocean

During two benthic research cruises carried out by AZTI-TECNALIA, two specimens of the spionid Paraprionospio coora Wilson, 1990 were collected. The genus Paraprionospio had not been previously reported from the Bay of Biscay, while the species P. coora is reported for the first time from the Atlantic Ocean. The specimens were found in circalittoral soft bottoms of the continental shelf of Basque coast (SE Bay of Biscay). In this paper, morphological descriptions, photographs, comments on the habitat, and geographical distribution of this species were provided.


Introduction
The global exchange of species has been accelerating in the last decades due to human transport (Thieltges 2005).Maritime traffic across and between the oceans and culturing of nonnative organisms at the edge of the sea has contributed to the spread and establishment of an ever increasing number of alien species in coastal and brackish water environments (Reise et al. 1999).These events can affect the biodiversity in newly settled areas, including in the Basque Country.
In recent years, the number of oceanographic surveys carried out along the Basque coast has increased considerably and substantially improved knowledge of the marine benthic fauna.Although most of these studies have a predominantly taxonomic character, some contributions about alien species have begun to appear (Ceberio et al. 1998;Martínez and Adarraga 2001, 2005, 2006, 2011;Martínez et al. 2006;Adarraga andMartínez 2011, 2012).
The phenomenon of the introduction of exotic organisms to the Basque coast affects all taxonomic groups but this study focussed on polychaetes.In the first general census of marine and estuarine alien species in the Basque Country, eighty-two alien and cryptogenic polychaete species, originally from tropical, subtropical, and temperate areas, were listed (Martínez andAdarraga 2005, 2006).Since then, we have identified three more cryptogenic species from circalittoral soft bottoms: the flabelligerid Diplocirrus stopbowitzi Darbyshire and Mackie, 2009, the scalibregmatid Axiokebuita cf.minuta (Hartman, 1967), and the cirratulid Chaetozone carpenteri (McIntosh, 1911).According to our research, Paraprionospio coora may be the most recent alien polychaete species detected in the Basque coast.
Paraprionospio was erected at the subgeneric level by Caullery (1914) to accommodate P. pinnata Ehlers, 1901, a Chilean species that was originally included in the genus Prionospio.The heterogeneous morphology of spionids that were grouped in this genus resulted in studies on the systematic position of the various forms included in it.With few exceptions (e.g., Söderström 1920;Light 1978), most researchers considered Paraprionospio at the generic level (e.g.Berkeley 1927;Foster 1971;Fauchald 1972;Blake and Kudenov 1978;Maciolek 1985;Blake 1996).The characteristic fusion of the prostomium, the arrangement of branchiae, their number and structure were considered characters of sufficient weight to warrant recognition at the generic level (Maciolek 1985).Following this approach, Paraprionospio is recognized today as a genus, member of the Prionospio generic complex that includes the genera: Aurospio Maciolek, 1981;Laubieriellus Maciolek, 1981;Orthoprionospio Blake and Kudenov, 1978;Prionospio Malmgren, 1867;andStreblospio Webster, 1879 (Sigvaldadóttir et al. 1997;Sigvaldadóttir 1998).
During two sampling campaigns recently carried out on the continental shelf of the Basque coast (SE Bay of Biscay), 234 species of polychaetes were identified, one of which was P. coora.This is the first record of P. coora in the Atlantic Ocean and the northernmost record in the world.
Originally described from the Pacific coasts of Australia (Wilson 1990), P. coora has recently been reported in the Mediterranean Sea from the Port of Valencia (Spain) as P. pinnata (Redondo and San Martín 1997), several sites in the Aegean Sea and the Sea of Marmara in Turkey (Yokoyama et al. 2010), and the Saronikos Gulf in Greece (Simboura et al. 2010).
Paraprionospio coora is a selective, surface deposit and suspension feeder that has been collected in a wide variety of habitats: estuaries, semi-enclosed bays, and the continental shelf.It can inhabit different sediment types in shallow water and circalittoral bottoms (Wilson 1990;Yokoyama and Choi 2010).

Study area
The Basque coast is located in the innermost part of the Bay of Biscay, between the west-east oriented coast of Spain and the north-south oriented coast of France.The two specimens were collected from soft-bottom sites on the continental shelf of the Basque Country (Figure 1, Table 1).This continental shelf is narrow, ranging from 7 km off Matxitxako Cape, to 20 km off the Oria River (Uriarte 1998).

Sample collection and analysis
Bottom samples were taken in 2010 and 2012 by AZTI-TECNALIA.One or three benthic replicates (depending on the program) were collected at each station using a Shipeck dredge (0.04 m 2 ) and a Smith-McIntyre dredge (0.1 m 2 ).The sediments were washed through a 1-mm mesh sieve, fixed with a 4% formalin solution, and stained with rose bengal.In the laboratory the samples were sorted and transferred to 70% ethanol.Afterwards, the fauna was identified to species or lowest possible taxon under an Olympus stereomicroscope and a Zeiss microscope.Specimens were measured using an ocular micrometer.Photographs were taken with a Nikon D50 digital camera adapted to an Olympus stereomicroscope and a Zeiss microscope.The two specimens of P. coora were temporarily stained with an alcoholic methyl blue solution.One specimen was deposited in the collections of the Museo Nacional de Ciencias Naturales de Madrid, Spain (Code MNCN 16.01/11288).
At each station, a supplementary sample was taken for sediment analysis.The granulometric analyses were carried out using a column of 8 sieves (4 mm to 31 µm).The percentages of gravel, sand, and mud were calculated as >2 mm fraction, 63 µm to 2 mm, and <63 µm, respectively (Holme andMcIntyre 1971 in Borja et al. 2006).The organic matter content was calculated using the ¨loss on ignition¨ method (Kristensen andAnderson 1993 in Borja et al. 2006).

Results
Two specimens of P. coora were identified, one in 2010 and one in 2012, from two stations in the SE Bay of Biscay (Figure 1) at depths 107 and 125 m.The substrate was muddy sand and mud (5.70 and 48.70% mud) with moderate organic matter content (2.50 and 2.78%).A total of 346 organisms were identified from these two sampling stations, belonging to 98 species or higher taxa.The annelids were numerically dominant with 76.01% of the total abundance.The molluscs comprised 11.27%, the arthropods 6.65%, and the other taxa accounting for 6.07% of the total  3 for details of the locations numbered 1 to 11. number of individuals.The trophic structure shows a dominance of surface-deposit feeders (69.36%), carnivores (17.63%) and subsurface-deposit feeders (7.80%).The more abundant species, the composition of the sediment, and ecological parameters at each station are summarised in Table 1.

SYSTEMATICS
Family SPIONIDAE Grube, 1850 Genus Paraprionospio Caullery, 1914 Paraprionospio coora Wilson, 1990 (Figure 2)  2A).Each peristomial wing with a small papilla on its posterior margin and some orange-brown pigmented patches on its lateral side.A pair of grooved palps with membranous basal sheath (Figure 2B).Three pairs of branchiae on chaetigers 1-3.First pair slightly longer than second ones; third pair clearly shorter (Figure 2C).Basal region of first branchial shaft with 4-5 conic processes placed along the anterior face (Figure 2D).All branchiae bearing lamellar plates enclosing lateral and posterior surfaces, in middle and distal regions flabellate.A small papilla present near base of third pair of branchiae (Figure 2E).Postsetal lamellae of notopodia long, foliaceous and pointed on the first three chaetigers and smaller and more rounded thereafter, from chaetiger 10 elevated, with increasingly triangular to lanceolate shape.Neuropodial lamellae prominent and pointed anteriorly on chaetigers 1-3, low and rounded posteriorly.Dorsal crests as well as semi-transparent dorsal cuticle absent.Granulate limbate capillary chaetae in both rami anteriorly, replaced by smooth, slender and non-limbate capillaries from about chaetiger 17 in the notopodium and from chaetiger 9 in the neuropodium.Hooded hooks appear in the neuropodia from chaetiger 9 accompanied by one or two inferior sabre chaetae.Notopodial hooded hooks from chaetigers 32-34.Individual hooks with 2-3 pairs of teeth above the main fang in the neuropodium (Figure 2F), and 2-3 pairs in the notopodium.Dorsum of chaetigers 12-17 with transverse series of lighter coloured, slightly raised ridges, 2 or 3 ridges per chaetiger.Pygidium with median long cirrus and two lateral short cirri (Figure 2G).

Remarks
Paraprionospio coora differs from all known species of the genus in lacking a semi-transparent dorsal cuticle.P. coora most closely resembles P. pinnata, but differs in having a papilla on the posterior margin of the peristomium, several conic processes in the basal region of the first branchial shaft, and a small globular papilla near the base of the third branchia (all these structures absent in P. pinnata).On the other hand, the branchiae in P. coora are noticeably different in length (similar in size in P. pinnata), and P. coora lacks the semi-transparent dorsal cuticle (present in P. pinnata).Another similar species is P. oceanensis.P. coora differs from P. oceanensis in lacking a filament at the base of the third branchia and lacking a semi-transparent dorsal cuticle.The number of anal cirri is also different, one in P. oceanensis and three in P. coora.

Ecology
Paraprionospio coora is an eurytopic species that is widely distributed in various water depths, sediments, and benthic community structures (Tamai 1985).Bathymetrically, it occurs in water 6 to 150 m deep (Wilson 1990;Yokoyama and Choi 2010).On the Japanese coast, it inhabits shallow waters and circalittoral soft bottoms, preferably on mud and sandy mud, both in sediments poor and rich in organic matter (Tamai 1985;Yokoyama et al. 2010).In Korea P. coora has been recorded in estuaries and environmentally degraded areas including: areas heavily impacted by an oil spill, organically enriched semi-enclosed bays, the outfall of a sewage treatment plant, a semi-enclosed harbour, and a dumping site on the continental shelf (Yokoyama and Choi 2010).The Greek specimens were reported on muddy sand circalittoral bottoms from a disturbed area (Simboura et al. 2010).In the present study, the specimens were collected in open sea, on the continental shelf in two stations characterized by moderate organic matter content.

Discussion
Basque specimens of P. coora agree well with the description and illustrations given by Wilson (1990).However, minor differences between our specimens and those from Australia have been observed.The number of apical teeth in neuropodial hooded hooks ranges between 2 and 3 pairs (only 2 pairs in the Wilson´s original description), and the interparapodial pouches were absent.Precisely these same discordant features were first pointed out by Yokoyama (2007) from Japanese specimens and later by Zhou et al. (2008) in China, Yokoyama and Choi (2010) in Korea, and Yokoyama et al. (2010) in specimens collected in the Mediterranean Sea (Table 2), so these authors suggest that both characters should not be used in distinguishing species, being taxonomically insignificant.This point of view is also accepted here.In this sense, the variability in number and arrangement of apical teeth has been pointed out by Blake (1996) and Ohwada and Nishino (1991) in others Spionidae species, like Apoprionospio pygmaea (Hartman, 1961) and Prionospio japonica Okuda, 1935.Similarly, the number of interparapodial pouches varies from zero to about 30 even in local populations of P. coora from Australia and East Asia (Yokoyama and Choi 2010).
The geographical distribution of P. coora is unclear.The confusion with other species, mainly with the type species P. pinnata, has contributed to this.The morphological characters treated by Ehlers (1901) in the original description of P. pinnata were rather general, so different forms were included in this single taxon, and consequently P. pinnata was regarded as a monotypic species (Foster 1971) with a cosmopolitan distribution (Light 1978;Maciolek 1985).However, the consideration of certain anatomical features previously ignored, such as the filament at the base of the third branchia, pigment papilla and spots on the peristomium, ventral bilobed flap on setiger 8 and transverse dorsal crests, has contributed to the discovery of several new species and improved the knowledge about the geographical distribution of other ones (Tamai 1981, Yokoyama and Tamai 1981, Wilson 1990, Yokoyama 2007).
In Japan P. pinnata was considered to be the only member of the genus Paraprionospio (Okuda 1937;Imajima and Hartman 1964) until Tamai (1981) and Yokoyama and Tamai (1981) pointed out that Japanese P. pinnata comprises four different morphological forms, which were later identified as P. coora, P. cordifolia, shows a preference for subtropical and warmtemperate regions (Table 3).This factor, together with its significant geographic separation in relation to the Basque coast and the improbability of taxonomic errors, leads us to suggest that this spionid could be another alien species that has arrived on the Basque coast.This current study represents the first record of specimens of this genus in the Bay of Biscay.The particular morphology of branchiae and their arrangement are features that make confusion with other species of the Prionospio complex unlikely.
In recent years, we have recorded in the Basque Country a considerable number of alien species from warm and subtropical areas (Martínez andAdarraga 2005, 2006;Adarraga andMartínez 2011, 2012).This is due, in part, to the biogeographic peculiarities of the Basque coast.The greater warming of the surface-water layer of the Bay of Biscay during the summer, compared to adjacent areas, favours the existence and acclimatization of southern species (Fischer 1938;Ibáñez 1978Ibáñez , 1985Ibáñez , 1989)).In the absence of marine farming areas near the area where the species has been collected, the most likely pathway for introduction is through the ballast water of a ship.It is most likely that the global nature of the shipping industry, with faster ships transporting large quantities of ballast between geographically separate areas, has an increasing potential to transport non-indigenous species to new areas (Leppäkoski et al. 2002).This way, there have been reported invasions of spionids in several regions (Bastrop et al. 1997;Çinar et al. 2005;Dagli and Çinar 2009), including the Basque coast (Martínez et al. 2006).
At the moment, we can not determine if this is a primary or secondary introduction.The possession of large, late-stage pelagic larvae in Paraprionospio species (about a month in P. patiens) (Tamai 1985), and their collection in oceanic waters suggests that this genus has a means for dispersal over long distances (Blake 1996).
Finally, regarding the effect of P. coora on the ecology of the Basque coast, we did not yet find any indication of an effect.The densities at the two stations are relatively low (8.33 and 10 ind./m 2 ).In particular, one of these stations (L-REF20) has been part of a monitoring program since 2000 and we have not observed any adverse impacts on macrofauna communities.Numbers of species, species diversity and community structure remain more or less the same.

Figure 1 .
Figure 1.Occurrence of Paraprionospio coora in the world and map of the study area with the two stations where this species was collected.See Table3for details of the locations numbered 1 to 11.

Table 1 .
Principal features for the two stations where Paraprionospio coora was collected.

Table 2 .
Main features of Paraprionospio coora from different areas of the world.

Table 3 .
Records of Paraprionospio coora in the world.