Recent studies and environmental legislation are involving sea pens in habitat conservation (OSPAR 2010, NOAA 2014, Kenchington et al. 2014). Despite their ecological value, pennatulacean coral habitats have been overlooked compared with cold-water coral ecosystems and studies of the latter mainly focus on stony corals (Order Scleractinia), sea fans and soft corals (Order Alcyonacea). Examples of sea pens forming fields (Aguilar et al. 2009, Porporato et al. 2014, Kenchington et al. 2014) and acting as nurseries for fish larvae (Pirtle 2005, Baillon et al. 2012) or as indicators of quality of mud habitats (MacDonald et al. 1996) highlight their role in benthic ecosystems. Like other corals, sea pens are slow-growing species that are particularly vulnerable because recovery after disturbances can take a long time (Kaiser et al. 2006, de Moura Neves et al. 2015). Moreover, in contrast with other corals, they are able to anchor in soft sediment (Hughes 1998), offering a shelter in a bare environment and acting as an indicator of the degradation of these sediments, which commonly sustain intensive fishing pressure or other disturbances (Thrush and Dayton 2002). The OSPAR Convention assessed the threatened habitat “sea pen and burrowing megafauna communities” in the northeast Atlantic affected by Nephrops trawling (Hughes 1998, Greathead et al. 2007, OSPAR 2010). Moreover, sea pens are involved in the soft-bottom coral garden habitat that is also considered threatened and/or declining (OSPAR 2008). Outside the OSPAR region, in eastern Canada, the important role of deep-sea pennatulacean corals as biogenic habitats has been reported (Kenchington et al. 2010, Baillon et al. 2014), and in the USA, under the reauthorized Magnuson-Stevens fishery Conservation and Management Act, deep-sea coral areas, including sea pens, have been protected from fishing (NOAA 2014). The Northwest Atlantic Fisheries Organization (NAFO) has also protected sea pen fields on the Flemish Cap.

After OSPAR recommendations to increase knowledge on the “sea pen and burrowing megafauna habitat” in areas where there are insufficient data and intensive fishing, such as the Cantabrian Sea (Sánchez and Olaso 2004, OSPAR 2010, ICES 2012), and under the European Marine Strategy Framework Directive (EU 2008) considerable advances in habitat definition have been made in Spain in the last few years, describing ‘the pennatulacean communities on circalittoral and bathyal soft bottoms’ in the North Atlantic Marine Area (MAGRAMA 2012). Despite these efforts, there is still limited information on this habitat in the area and it receives little attention and protection.

In the Bay of Biscay and nearby areas, 21 species of sea pens have been reported, 13 of them occurring off Spain south of the 44°N parallel (Altuna 2010, Supplementary Material Table S1). During several surveys undertaken every autumn by the Spanish Institute of Oceanography (IEO) in the Cantabrian Sea (southern sector of the Bay of Biscay) and off Galicia, five of these species, Funiculina quadrangularis, Pennatula aculeata, Pennatula phosphorea, Pteroeides spinosum and Veretillum cynomorium, were found on circalittoral and upper bathyal soft bottoms, sometimes in abundance. Although some of these species are of conservation significance (Hughes 1998, OSPAR 2010), knowledge of them is uneven in this area, with little information on their abundance, distribution and habitat requirements.

F. quadrangularis has a worldwide range, being common throughout the North Atlantic and the Mediterranean Sea (Manuel 1981, Gili and Pagès 1987), with a wide bathymetric range from 20 m to depths of over 3000 m (Tixier-Durivault and d’Hondt 1975, Manuel 1981, López-González et al. 2001). It is a sensitive species considered to be of conservation significance. This species is reported to be especially vulnerable to disturbances because of its inability to withdraw rapidly into the sediment (Hughes 1998). According to the European Nature Information System (EUNIS), it is a characterizing species of the circalittoral biotope ‘sea pen and burrowing megafauna’, as well as being common in the bathyal facies of soft muds associated with Aporrhais serresianus in the Mediterranean Sea. Furthermore, with the implementation of the MSFD in Spain, specifically in the North Atlantic Marine Area (MAGRAMA 2012), this species is also described as a characterizing species of ‘the pennatulacean communities on circalittoral and bathyal soft bottoms’ in the northern Atlantic Spanish area.

The genus Pennatula has a worldwide distribution (Williams 2011), and three out of the five species listed by Williams (2014) from the European Register of Marine Species area occur in the Cantabrian Sea off Spain: namely P. aculeata, P. grandis and P. phosphorea. Records of P. rubra from this area are misidentifications. The species P. aculeata and P. phosphorea are often uncertainly classified (Manuel 1981), and the latter has been confused with other species (Hughes 1998). Thus, tracing their distributions is not easy despite the fact that they are accepted species (Williams 2014). Both species may co-occur in some areas and at some depths in the southern sector of the Bay of Biscay and Galicia (Supplementary Material Table S1). P. phosphorea is widespread in the North Atlantic and in the Mediterranean Sea, with several records from the whole Bay of Biscay (Tixier-Durivault and d’Hondt 1975, Gili and Pagès 1987), and is also involved in conservation issues (OSPAR 2010). According to EUNIS classification, it occurs together with Virgularia mirabilis in the biotope ‘sea pen and burrowing megafauna’ in the North and Irish Sea, but also in the facies of sticky muds with V. mirabilis in the Mediterranean Sea. It may also be found in the biotope ‘Myrtea spinifera and polychaetes in offshore circalittoral sandy mud’ in the North and Irish Sea.

On the other hand, P. aculeata has been mainly reported in the North Atlantic, including the Bay of Biscay, but there are some Mediterranean records as well (Tixier-Durivault and d’Hondt 1975, Langton et al. 1990, Ocaña et al. 2000). A review of the literature (Supplementary Material Table S1) indicates that it can reach deeper depths than P. phosphorea in the Bay of Biscay and nearby areas, and it has not been associated with a given habitat.

The two genera Pteroeides and Veretillum are reported in the eastern Atlantic and West Pacific and described to be bathymetrically restricted to shallow waters (Williams 2011). Specifically, the geographical distribution of P. spinosum and V. cynomorium ranges from the Bay of Biscay to the Atlantic shores of Africa, including the Mediterranean Sea (Gili and Pagès 1987, López-González et al. 2001, Altuna, 2010). They are involved in the habitat ‘the pennatulacean communities of circalittoral and bathyal soft bottoms’, according to the description of the biodiversity in the North Atlantic Marine Area (MAGRAMA 2012) with the implementation of the MSFD.

The present work considers the biology and ecology of the most abundant sea pens on the shelf and in the upper bathyal of the southern Bay of Biscay and northwestern Spain (Galicia), mapping their distribution, identifying significant concentrations and describing the benthic/demersal communities associated with them.

Our results provided further evidence of sea pens in the southern Bay of Biscay. Pennatulaceans have been previously reported in the area, not only in the proposed MPAs on the Galicia Bank (IEO 2014a) and in the Avilés Canyon (IEO 2014b), but also in the inner basin of the Le Danois Bank MPA (BOE 2011) and in Galician waters (Aguilar et al. 2009). Moreover, under the MSFD, Spain has recently identified pennatulacean communities as the most diverse and richest habitats on circalittoral and bathyal soft bottoms of the northern Atlantic Spanish area (MAGRAMA 2012). Our results also provided further evidence of sea pens forming aggregations on the northern Atlantic Spanish shelf. Although sea pens were broadly found at low density in the study area, the aggregations with a noteworthy high density in the central part of the Cantabrian Sea and in the southern Galician area and the high spatial autocorrelation among near samples supports the hypothesis of sea pens forming aggregations in the area. The hotspots in the Cantabrian Sea were of the species F. quadrangularis, while in the Galician area they were of Pennatula spp. Though the sea pens V. cynomorium and P. spinosum were scarce, they showed two hotspots in the southern Galician area and in the easternmost area of the Cantabrian Sea, respectively.

In addition, differences in the distribution of sea pen aggregations were supported by the fact that longitude was among the variables contributing most to the differentiation of the aggregations. This factor is a result of environmental differences between the western (Galicia area) and eastern (Cantabrian Sea) zones of the study area, the Galician and Cantabrian Sea, respectively. In general, there is higher primary production in Galician waters (López-Jamar et al. 1992, OSPAR 2000) and, in particular, a heterogeneous grain size and a higher OM content have been reported to the south of Cape Finisterre (López-Jamar et al. 1992), where Pennatula spp. was highly abundant. Pennatula spp. are known to be much stouter and fleshier than F. quadrangularis (Manuel 1981), which probably helps them to settle in less homogeneous sediments. In fact, both species are known to occur in muddy substrata, but Manuel (1981) also reported P. phosphorea in sandy substrata and Greathead et al. (2015) reported the absence of F. quadrangularis in sediment with gravel content above 30%.

In addition, longitude also means differences in topography, which leads to an apparent absence of aggregations of sea pens on the narrow shelf and steep slope of the eastern part of the Cantabrian Sea, with the exception of the easternmost shelf area. Therein, mud deposits (Jouanneau et al. 2008) could be supporting the settlement of the few aggregations of F. quadrangularis.

On the other hand, depth was also an influential factor in the distribution of the sea pens in the study area. The few aggregations of P. spinosum and V. cynomorium were found at about 50 m depth, although some specimens were recorded at unusual depths in the area if compared with data in the literature (Supplementary Material Table S1). We found that 70% of the occurrences of V. cynomorium in our study area were detected above 100 m and three colonies were even found at an unusual depth of 372 m, despite the fact that these two species are known to be continental-shelf species with a distribution related to terrigenous sediments (Gili and Pagès 1987, Williams 2011, Sardá et al. 2012). López-González et al. (2001) reported, in the eastern Atlantic, a wider depth range (25-188 m) than Williams (1990, 13-91 m), and Gili and Pagès (1987) showed an even deeper limit in the Mediterranean Sea (around 260 m). However, neither of them mentioned such a deep distribution for the species. In addition to this interesting result, the highest aggregation of colonies of V. cynomorium (118 colonies), together with some colonies of P. spinosum (19 colonies), were found near the Arousa Ría (Galicia, Spain), where fields of V. cynomorium have been previously reported (Fernández et al. 2005, Aguilar et al. 2009). This result provides further evidence of sea pens forming aggregations, widely recognized as key benthic habitats (OSPAR 2008, DFO 2010, Kenchington et al. 2011).

Another result of the influence of depth on the distribution of sea pen species was found in the Galician area, where Pennatula spp. was abundant from 100 to 200 m, while the few occurrences of F. quadrangularis were mainly between 200 and 300 m. Hughes (1998) and Greathead et al. (2007) also suggest the preference of F. quadrangularis for deeper habitats where the conditions may be more stable. In addition, also relating depth to sediment particle size and organic content, finer and organic-rich sediments have been reported on the inner shelf off the Rías Bajas (Galicia, Spain), where Pennatula spp. was more abundant, while on the outer shelf the sediments are sandier and have low organic content (López-Jamar et al. 1992). Nevertheless, Greathead et al. (2007) suggest that depth is a more important factor than sediment type in the distribution of F. quadrangularis.

Tracing the distributions and bathymetric ranges of P. phosphorea and P. aculeata in the Bay of Biscay and nearby areas from the literature is not easy, as we highlighted in the Introduction. However, our results provide evidence of different bathymetric distributions between the two species. Hence, the fact that P. aculeata extends deeper than P. phosphorea suggests that the aggregations of Pennatula spp. found in the study area do not include specimens of P. aculeata but only of P. phosphorea, although more data are still sorely needed. P. aculeata has also been found at similar depths in the southern Bay of Biscay, as a result of the bathyal surveys carried out by the ECOMARG project (www.ecomarg.com). During these surveys, P. aculeata was found only at 745 and 761 m in the Le Danois Bank MPA, at 786 m on the Galicia Bank (northwestern Spain) and at 828 m in the Avilés Canyon (northern Spain) (A. Altuna, personal communication). All these records of upper bathyal presence of P. aculeata, and to a large extent, the lack of reliable data of P. phosphorea from these areas, highlight the need for more research on the bathymetric distribution and ecological needs of these two species.

With respect to the sampling of sea pen communities in the southern Bay of Biscay, the present study adds long-term information on the distribution of sea pens in an extensive area, despite the use of trawling sampling. Techniques such as beam trawl and demersal otter trawl are often used in benthic community studies, although monitoring is extensively recommended for the management of sea pens and burrowing megafauna (Hughes 1998, Greathead et al. 2007). Monitoring and assessment of vulnerable habitats have been carried out in the area with non-destructive monitoring techniques such as remotely-operated vehicles and photogrammetric sledges (Aguilar et al. 2009, www.ecomarg.com, Sánchez et al. 2009), but they were short-term or spatially isolated studies. In addition, sampling of some sea pen communities is not easy and very inaccurate, as some pennatulaceans can withdraw below the sediment surface and bias the results of monitoring. The density of some such sea pens in a given area can change by over 200% in a few hours (Birkeland 1974). Virgularia mirabilis is known to withdraw into the sediment and P. phosphorea and P. aculeata are also able to do so, although not as quickly, but F. quadrangularis, P. spinosum and V. cynomorium do not show this feature (Langton et al. 1990, Hughes 1998).

The species composition of the aggregations of sea pens in the study area agrees with previous studies in the area, which showed depth as a key factor structuring communities (Olaso 1990, Serrano et al. 2006). Many species that occur in the aggregations of F. quadrangularis and Pennatula spp. coincided with the eurybathic species described in the area by Olaso (1990), such as the portunid crab Liocarcinus depurator, the spider crab Macropodia longipes and the sea snail Neptunea contraria, or with the characteristic species of the shelf (between 140 and 300 m), such as the sea anemone Actinauge richardi, the sea snail Ranella olearium and the sea cucumber Parastichopus regalis. Specifically in the shallower samples of F. quadrangularis, the higher-contributing species Astropecten irregularis, Eledone cirrhosa, Pagurus prideaux and Leptometra celtica were reported by Olaso (1990) on the upper edge of the shelf (between 90 and 140 m), whereas the anomuran Munida sarsi, as the most abundant and the highest-contributing species in the deeper samples of F. quadrangularis, was reported as a dominant species on the shelf. This author compared the different distribution of M. sarsi with the other common anomuran in the area, Munida intermedia and described both species as dominant species on the shelf, but M. sarsi showed greater density at 275 m in the Cantabrian Sea, and M. intermedia showed greater density at 175 m in the Galician area. This explains the higher abundance of M. sarsi in the deeper aggregations of sea pens in the area and the greater occurrence of M. intermedia in the aggregations of Pennatula spp., which are mainly distributed in Galician waters. In addition, Olaso (1990) and Serrano et al. (2006) showed depth and sediment characteristics to be priority factors determining species composition.

Large differences were found between the aggregations described in the present study and the habitat “sea pen and burrowing megafauna communities” defined by OSPAR. This habitat was reported in the North Sea, the Irish Sea and the Bay of Biscay and may include populations of V. mirabilis, P. phosphorea or F. quadrangularis with burrowing crustaceans such as Nephrops norvegicus, in fine mud at depths of between 15 and 200 m. In the southern Bay of Biscay, we found aggregations of F. quadrangularis on circalittoral soft bottoms but also on the upper bathyal deeper than 200 m. In addition, we also found aggregations of Pennatula spp. in the Galician area, all of them on circalittoral bottoms. Finally, V. mirabilis was absent and N. norvegicus was found at low densities in the study area, despite its general distribution between 90 and 600 m in the study area (ICES 2012). Other species not mentioned by OSPAR, M. sarsi, A. irregularis, L. depurator, Ophiura ophiura and M. intermedia, were frequent in the aggregations found in the study area. Although the southerner area and the deeper and trawling sampling in the present study marked differences from the methodology used to define this habitat in Northern Europe, and the community composition and density of the aggregations of sea pens on the northern Spanish shelf might be biased by some other factors.

Some of these frequent species, L. depurator, O. ophiura and A. irregularis, are known to be opportunistic species in trawled areas (Kaiser et al. 1998, Vergnon and Blanchard 2006, de Juan et al. 2007) like our study area which support an intensive fishing pressure (Sánchez and Olaso 2004, ICES 2012). In contrast to the North Sea, the Irish Sea and northern Bay of Biscay, where Nephrops is one of the most important fisheries, in the southern Bay of Biscay N. norvegicus has stopped being a target species over time due to its low abundance. Nevertheless, it is a valued component of the mixed bottom trawl fishery together with hake, anglerfish, megrim, horse mackerel, mackerel and blue whiting (Fariña and Herraiz 2003, Punzón et al. 2010, ICES 2012). The Nephrops stock is declining in the study area (Fariña and Herraiz 2003) and recovery plans were adopted in 2005 (Council Regulation (EC) 2166/2005). This decline in Nephrops stock could have coincided with a decline in sea pens in the past, which could partially explain the low densities of sea pens found in the study. Now, this mixed bottom trawling could be a similar threat for sea pens in the Cantabrian and Galician waters to that of Nephrops trawling in the North Sea, the Irish Sea and the northern Bay of Biscay, but this possibility has not been assessed. Evidences like the intensive fishing pressure, the declining Nephrops stock, the presence of opportunistic species in the aggregations and the low densities of sea pens found in the present study suggest that trawling might be affecting sea pen abundance in the southern Bay of Biscay and highlight the need for further information to assess the status of these important communities in this region.