Patterns of Bathymetric Zonation of Bivalves in the Porcupine Seabight and Adjacent Abyssal Plain, NE Atlantic

ARTICLE IN PRESS

Deep-Sea Research I 52 (2005) 15–31 www.elsevier.com/locate/dsr

Patterns of bathymetric zonation of bivalves in the Porcupine Seabight and adjacent Abyssal plain, NE Atlantic

Celia OlabarriaÃ

Southampton Oceanography Centre, DEEPSEAS Benthic Biology Group, Empress Dock, Southampton SO14 3ZH, UK

Received 23 April2004; received in revised form 21 September 2004; accepted 21 September 2004

Abstract

Although the organization patterns of fauna in the deep sea have been broadly documented, most studies have focused on the megafauna. Bivalves represent about 10% of the deep-sea macrobenthic fauna, being the third taxon in abundance after polychaetes and peracarid crustaceans. This study, based on a large data set, examined the bathymetric distribution, patterns of zonation and diversity–depth trends of bivalves from the Porcupine Seabight and adjacent Abyssal Plain (NE Atlantic). A total of 131,334 individuals belonging to 76 species were collected between 500 and 4866 m. Most of the species showed broad depth ranges with some ranges extending over more than 3000 m. Furthermore, many species overlapped in their depth distributions. Patterns of zonation were not very strong and faunal change was gradual. Nevertheless, four bathymetric discontinuities, more or less clearly delimited, occurred at about 750, 1900, 2900 and 4100 m. These boundaries indicated ﬁve faunistic zones: (1) a zone above 750 m marking the change from shelf species to bathyal species; (2) a zone from 750 to 1900 m that corresponds to the upper and mid- bathyalzones taken together; (3) a lowerbathyalzone from 1900 to 2900 m; (4) a transition zone from 2900 to 4100 m where the bathyal fauna meets and overlaps with the abyssal fauna and (5) a truly abyssal zone from approximately 4100–4900 m (the lower depth limit of this study), characterized by the presence of abyssal species with restricted depth ranges and a few specimens of some bathyalspecies with very broad distributions. The 4100 m boundary marked the lower limit of distribution of many bathyal species. There was a pattern of increasing diversity downslope from 500 to 1600 m, followed by a decrease to minimum values at about 2700 m. This drop in diversity was followed by an increase up to maximum values at 4100 m and then again, a fall to 4900 m (the lower depth limit in this study). r 2004 Elsevier Ltd. All rights reserved.

Keywords: Bivalves; Zonation patterns; Vertical distribution; Diversity; Deep sea; NE Atlantic

ÃDepartamento de Ecoloxı´ a e Bioloxı´ a Animal, Area Ecologı´ a, Universidad de Vigo, Campus Lagoas-Marcosende, 36200 Vigo (Pontevedra), Spain. Tel.: +34 986 812588; fax: +34 986 812556. E-mail address: [email protected] (C. Olabarria).

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1. Introduction may help to elucidate the factors driving these patterns. Although zonation of fauna, i.e. change of In the Porcupine Seabight and adjacent areas species composition with depth, in the deep sea diverse zones of faunalchange have been consis- have been broadly documented (see Howell et al., tently reported. In general, though with important 2002), most studies have dealt only with the local variations, a first boundary related to the megafauna (see Cartes et al., 2003; Cartes and water mass structure and permanent thermocline Carrasson, 2004). Different faunalzones, i.e. occurs at 700 m depth (e.g. Gage, 1986; Howell regions of lesser faunal change bounded by regions et al., 2002). A second faunalturnover associated of greater faunalchange, have been proposed in with changes in currents occurs at 1100 m the deep sea, but there is still some disagreement (Howell et al., 2002). In addition, there is a third over the terminology of these zones (see for review boundary at about 1700 m marked by a rapid Howell et al., 2002) and their bathymetric limits. faunalchange and relatedto changes in tempera- Faunalboundaries reported in the literature ture and water masses (Gage, 1986; Billett, 1991; vary depending on the taxonomic group consid- Howell et al., 2002). Finally, there is a boundary at ered (e.g. Vinogradova et al., 1959; Rowe 3000 m that separates bathyaland abyssalfauna and Menzies, 1969; Rex, 1973, 1981; Gage et al., (Lampitt et al., 1986; Billett, 1991; Howell et al., 1985; Billett, 1991; Howell et al., 2002). Faunal 2002). This zonation scheme is based on studies of zonation appears to be more apparent in higher megafaunalgroups, whereas smallermacrofauna trophic levels, e.g. fish and crustaceans, than in has been generally neglected. Studies focusing on lower trophic levels, such as polychaetes or macrofaunal assemblages belonging to lower bivalves (see Cartes et al., 2003; Cartes and trophic levels, e.g. polychaetes, gastropods or Carrasson, 2004). bivalves, could contribute to a better understand- Many of the previous studies focused on general ing of the structure of deep-sea communities in this faunalzonation patterns (e.g. Rowe and Menzies, area. 1969; Ohta, 1983), or on the zonation of specific Bivalves represent about 10% of the deep-sea taxonomic groups (e.g. Rex, 1977; Southward, macrobenthic fauna, being the third taxon in 1979; Carney and Carey, 1982; Gage, 1986; abundance after polychaetes and peracarid crus- Billett, 1991; Cartes and Sarda` , 1993; Howell et taceans (Allen and Sanders 1996). Deep-sea al., 2002). Such studies have revealed that there is bivalves have been studied largely from a faunistic replacement of species with depth and that most of and taxonomic point of view (e.g. Knudsen, the species show restricted depth ranges (e.g. 1970; Sanders and Allen, 1973; Allen and Murray, 1895; Rex, 1977; Carney et al., 1983; Turner, 1974; Allen and Morgan, 1981; Allen Etter and Rex, 1990; Howell et al., 2002). Causes and Hannah, 1989; Allen 1998). Studies on of this zonation have been attributed to physical the diversity patterns of deep-sea bivalves have and/or biological factors such as temperature been also reported from a number of areas (e.g. (Rowe and Menzies, 1969), pressure (Young et Rex, 1981; Grassle and Maciolek, 1992; Rex et al., al., 1996), hydrographic conditions and topogra- 1993, 1997, 2000; Allen and Sanders, 1996). phy (Lampitt et al., 1986; Rice et al., 1990), Nevertheless, few studies have investigated pat- nutrient input (Rex, 1981; Rice et al., 1990), terns of bathymetric distribution and zonation of larval dispersal (Rowe and Menzies, 1969; bivalves in detail (but see Allen and Sanders, Billett 1991), competition, predation and trophic 1996). level (Rex, 1977, 1981; Cartes and Sarda` , This study, based on a large data set, examines 1993). Nevertheless, the causes for the change in the bathymetric distribution of bivalves from the species composition with depth are complex Porcupine Seabight and adjacent AbyssalPlain and severalfactors might act to produce the (NE Atlantic), patterns of zonation and diversi- observed pattern. Therefore, detailed studies of ty–depth trends. Possible causes of these patterns bathymetric distribution of deep-sea organisms are also discussed. ARTICLE IN PRESS

C. Olabarria / Deep-Sea Research I 52 (2005) 15–31 17

2. Material and methods materialare accumulated.No sediment fan is evident where the channelopens onto the Abyssal 2.1. Study area Plain, indicating either little detrital material is transported or that such materialis distributed The Porcupine Seabight and Porcupine Abyssal once it reaches the AbyssalPlain( Rice et al., Plain are located more than 200 km to the south- 1991). west of Ireland (Fig. 1). The Porcupine Seabight is an amphitheatre-shaped embayment in the con- 2.2. Collection and treatment of samples tinentalmargin to the southwest of Ireland,and its sides slope steadily from the edge of the Irish Shelf A totalof 76 epibenthic sledgeand 50 otter at 200 m down to a depth of about 4000 m (site trawl samples was collected between 500 and described in Rice et al., 1991). The Seabight opens 4866 m over a period of 22 years. These samples onto the Porcupine AbyssalPlainthrough a were taken during the Institute of Oceanographic relatively narrow entrance to the southwest (Rice Sciences (IOS) biology programme in the Porcu- et al., 1991). The Porcupine Abyssal Plain lies pine Seabight and adjacent AbyssalPlainbetween south of the Rockall Trough and north of the November 1977 and December 1986 (Rice Iberian AbyssalPlain,at a depth between 4000 et al., 1991) and during the BENGAL programme and 5000 m. The Seabight is bound on its west and on the Porcupine AbyssalPlainbetween Septem- northwest side by the Porcupine Bank and on its ber 1995 and October 1998 (Billett and Rice, south and southeast side by the Goban Spur, 2001). Despite this extensive sampling programme, leaving a narrow entrance. The western slopes of there were severalgaps in the data set ( Fig. 2) the Porcupine Seabight are steeper than the that might affect the outcome of this study. eastern slopes. The eastern slope of the Seabight Nevertheless, many depth bands were represented differs markedly from the western one because of by more than 3 sampling runs (sledge and the presence of many channels, which coalesce to OTSB), so data were reliable and produced a form a single large channel or canyon running quite comprehensive representation of species through the Seabight. The channels are still areas distribution. of active transport where large amounts of detrital The IOS epibenthic sledge (Rice et al., 1982) carries an acoustic monitor, which transmits information on the behaviour of the sledge on the seabed. The semi-balloon otter trawl (OTSB) (Merrett and Marshall, 1981) has an acoustic beacon mounted on one of the trawldoors to provide better estimates of the length of the tow. Mercury tilt switches in this monitor indicate the arrivaland departure of the net at the seabed. Therefore, the area of seabed sampled was calculated from the width of the sledge/trawl opening and distance of the sampling run over the seabed. Nevertheless, the epibenthic sledge and the semi-balloon otter trawl, OTSB, have some shortcomings depending, to a large extent, on the faunalgroup under study (see for review Howell et al., 2002). For example, the otter trawl shows a ﬁshing efﬁciency of 68% for larger megabenthos (Bett et al., 2001), but it does not provide reliable quantitative samples for epibenthic fauna or Fig. 1. Location of the study area and sampling stations. infauna. Despite the shortcomings, samples collected ARTICLE IN PRESS

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2.3. Data treatment

To analyse the bathymetric distributions of species, sledge and trawl samples were grouped into 100 m depth bands. Mean abundances per 100 m depth band were calculated for each species and then converted to percentage of relative abundance (Bett, 2001). Epibenthic sledge data were used where possible and supplemented by OTSB data where sledge data were lacking. As a relative measure of abundance was used, as opposed to absolute abundances, this was not a problem in the data analysis. The range of a species was assumed to be continuous between the depths of first and last occurrence. To investigate species change with depth, both OTSB and sledge data were used together to give depths of first and last occurrence of species. These values were then used to produce plots of species addition, loss and succession with increasing depth in order to identify possible boundaries where faunalturnover occurs, i.e. zonation patterns. To identify the main assemblages, both sledge and trawldata were transformed into presence/ absence data (Clarke and Warwick, 1994) in order to combine data from the two sampling gears. This qualitative approach was adopted in an attempt to avoid the bias introduced by the use of different samplers. Samples were then grouped into 500 m Fig. 2. Distribution of (A) sledge, (B) OTSB sampling effort in depth bands and labelled D1–D9. This grouping the Porcupine Seabight and AbyssalPlainin 100 m depth allowed the data to be investigated in terms of bands. Grey bars: total number of samples collected in that depth rather than species change (see Howell et al., particular depth band; black bars: samples containing bivalves. 2002). The Sorenson similarity coefficient (Clarke and Warwick, 1994) was applied to the transformed grouped data to obtain a similarity matrix. in this area over this long period of time provided an Subsequently, hierarchical clustering with group- important data set in order to get better under- averaged linking and non-metric multi-dimen- standing of patterns of distribution of species and sional scaling using the similarity matrix were processes driving these patterns in the northeast performed. To test the relationship between depth Atlantic Ocean. and change in species composition a Spearman’s Samples were sorted on deck and fixed in borax- rank correlation coefficient was calculated for the buffered 4% formaldehyde in seawater and then x-ordinate of the MDS plot and depth. preserved in 80% alcohol. Specimens were identi- Diversity was analysed with the rarefaction fied to species level when possible. A total of method (Hurlbert, 1971). Values for the expected 131,334 individuals belonging to 76 species were number of species in a sample of 50 individuals collected. The number of species in each sample were extracted from the programme PRIMER was determined per sample and numerical density (Plymouth Routines in Multivariate Ecological was standardized to 100 m2. Research, ver. 5), and a graph of expected number ARTICLE IN PRESS

C. Olabarria / Deep-Sea Research I 52 (2005) 15–31 19 of species against depth was plotted. The ES (50) Furthermore, various species co-occurred at value was used in this study because of the patchy their maximum abundances at a particular depth distributions of species and low abundances of (see 2700–2800 m depth band; Table 1). Although many of them. Sledge and OTSB data were some species’ verticalranges were broad, their combined after separate analyses indicated similar relative abundance patterns changed markedly results from both gears individually. below 2500 m. For example, Ledella pustulosa marshalli, Malletia obtusa and K. atlantica were more abundant below this depth (Fig. 2), whereas 3. Results P. lucidum and Limatula sp1. decreased in abundance. 3.1. Species distribution Faunaldiscontinuities occurred at 2000– 2500 m and 3100–3500 m. Very few species were In general, most of species showed a broad present, and none occurred in large numbers (but depth range with some species’ ranges extended see Idas cf argenteus and Xylophaga sp1). These over more than 3000 m (e.g. Pristigloma nitens, depths correspond to gaps in the data set (Rice et Thyasira equalis, Kelliella atlantica, Abra profun- al., 1991; Howell et al., 2001) and a rocky area dorum and Cuspidaria obesa; Table 1, Fig. 3). (3000–3500 m) at the base of the continental Although there was a very gradual replacement of slope. species with depth (Fig. 3) many species overlapped in their depth ranges, i.e. approximately 3.2. Assemblages and patterns of zonation 62% of species coexisted in the 2600–3000 m depth range. A high percentage (67%) of species Both Hierarchical Cluster Analysis and MDS occurred deeper than 3000 m, whereas 21% of evidenced an arrangement of stations in 5 different species occurred shallower than 2000 m (Table 1). groups (Figs. 5 and 6). These groups (A, B, C, D Only sixteen species showed comparatively narrow and E; Fig. 5) were very dissimilar to each other depth ranges (o300 m) (Table 1) and most of them (similarity close to zero). Although a Spearman’s occurred shallower than 1700 m (but see Nucu- rank correlation of depth with the MDS-ordinate lana sp1, Ledella aberrata, C. circinata, Halonym- gave a significant result (0.64; po0.0001), some pha sp1, Edentaria similis; Table 1). Despite most samples from different depths were grouped species having broad bathymetric ranges, some together (for example, group A). Despite the zones of enhanced species turnover were identified arrangement of the stations according to a depth (Fig. 4). gradient there was also some indication of Most of species showed a patchy distribution alongslope organization within area of study (see through their depth range, often occurring, in any assemblages; Fig. 7). Most species with broad great abundance, only over a very narrow depth bathymetric ranges were widespread in the area range of 100–300 m (Fig. 3). The narrow depth of (e.g. Thyasira obsoleta, Polycordia gemma, Yol- greater abundance did not generally occur in the diella sp1; Fig. 8); however, a few species showed middle of their total depth ranges (Table 1; Fig. 3). more restricted horizontaldistributions (e.g. Pro- For example, species such as Bathypecten eucyma- pamussium centobi, Yoldiella inconspicua; Fig. 9). tus, Similipecten similis, Parvamussium permirum, Nevertheless, four more or less clearly delimited A. profundorum, L. ultima and Cardiomya knudseni bathymetric boundaries could be found. An upper reached their respective relative high levels of slope zone from 500 to 750 m could be identified abundance at the start or end of their depth by both cluster and MDS analysis (cluster E, Figs. ranges. In contrast, few species (e.g. Malletia cf 5 and 6). The rate of species succession was abyssorum, Verticordia cf triangularis, Yoldiella gradualin this region with an addition of 8 species sp1, K. atlantica) presented their maximum that extended throughout the area and beyond abundances in the middle of their total depth (but see Chlamys sp2) (Fig. 3). Two species typi- ranges. fied this zone, Chlamys sp1 and Chlamys sp2. ARTICLE IN PRESS

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Table 1 The depth distribution of bivalve species from the Porcupine Seabight and the Porcupine Abyssal Plain

Species Depth range Depth of maximum Species Depth range Depth of maximum (m) abundance (m) (m) abundance (m)

Deminucula atacellana d 1200–1800 1200–1400 Parvamussium permirum 1600–4900 1600–1700 Nuculoidea bushae d 700–2900 900–1000 Propamussium centobi 1300–4900 2700–2800 Brevinucula verrilli d 2600–4100 2700–2800 Limatula sp1 700–2800 1100–1200 Nuculoma granulosa d 1600–1700 1600–1700 Limatula sp2 2700–4900 3900–4000 Pristigloma nitens d 900–4000 2600–2700 Axinodon sp1 1200–3600 1200–1300 Nuculana sp1 d * 4800–4900 4800–4900 Thyasira equalis d 1200–4900 1200–1300 Ledella aberrata d 4800–4900 4800–4900 Thyasira eumyaria d 900–1500 900–1000 Ledella pustulosa 1600–4100 2700–2800 Thyasira ferruginea d 500–2700 500–600 marshalli d Ledella pustulosa 1300–2700 1600–1700 Thyasira granulosa d 900–1000 900–1000 pustulosa d Ledella ultima d 1900–4900 4800–4900 Thyasira inﬂata d 1200–3600 2600–2700 Spinula ﬁlatovae d 1100–4100 1300–1400 Thyasira obsoleta d 900–4100 1200–1300 Spinula hilleri d 1400–4100 2700–2800 Thyasira pygmaea d 2600–2700 2600–2700 Spinula subexcisa d 1100–3600 1100–1200 Thyasira sp1 d 900–2800 900–1000 Silicula fragilis d 4000–4900 4800–4900 Thyasira succisa succisa d 1100–3600 1900–2000 Malletia cf abyssorum d 2600–4900 3900–4000 Thyasira ultima d 1600–1700 1600–1700 Malletia cuneata d 900–4900 4000–4100 Kelliella atlantica s 500–4900 2600–2700 Malletia obtusa d 1400–4000 3900–4000 Mysella sp1 1200–3100 1300–1400 Neilonella whoii d 3000–4900 3000–3100 Abra profundorum * d 700–4900 700–800 Neilonella saliciensis d 500–4000 2600–2700 Abra sp1 d 500–1300 500–600 Yoldiella sp1 d 900–4900 2700–2800 Xylophaga sp1 2000–2500 2000–2100 Yoldiella inconspicua d 700–4000 700–800 Lyonsiella abyssicola c 1100–1400 1100–1200 Yoldiella jeffreysi d 700–4000 1400–1500 Lyonsiella formosa c 1100–1700 1100–1200 Yoldiella semistriata d 1600–2000 1900–2000 Lyonsiella subquadrata c 900–2800 1200–1300 Bathyarca glacilis * 900–1000 900–1000 Verticordia cf triangularis c 3000–4400 3500–3600 Bathyarca inaequisculpta 3500–4900 3900–4000 Policordia cf gemma * c 900–4900 1100–1200 Bathyarca nodulosa * 800–900 800–900 Cuspidaria atlantica c 900–4100 3500–3600 Limopsis minuta 600–1700 1300–1400 Cuspidaria circinata c 4000–4100 4000–4100 Limopsis tenella 2600–4900 2700–2800 Cuspidaria obesa c 600–4900 1100–1200 Dacrydium ockelmanni s 1100–4900 1600–1700 Cardiomya costellata * c 700–1400 1300–1400 Idas cf argenteus s 1100–3700 2400–2500 Cardiomya knudseni * c 900–4000 3900–4000 Chlamys sp1 * s 500–900 700–800 Myonera atlantica c 500–4900 1300–1400 Chlamys sp2 s 500–700 600–700 Rhinoclama notabilis c 1400–4600 4000–4100 Cyclopecten 800–4900 3900–4000 Tropidomya abbreviata * c 800–900 800–900 ambiannulatus s Delectopecten vitreus s 500–4100 1200–1300 Halonympha sp1 * c 4800–4900 4800–4900 Hyalopecten undatus s 2700–4100 2700–2800 Protocuspidaria verityi c 1300–4900 2700–2800 Bathypecten eucymatus s 1100–4000 1100–1200 Edentaria simplis c 2700–2800 2700–2800 Similipecten similis s 700–3700 700–800 Poromya granulata c 1300–3700 1300–1400 Parvamusium lucidum s 1100–3600 1600–1700 Poromya tornata c 800–4900 3900–4000

*Taken from OTSB data. sSpecies considered as suspension feeder; dspecies considered as deposit feeder; cspecies considered as carnivore.

Nevertheless, the existence of this boundary at A bathyalzone extended from 750 to 1900 m. 750 m should be interpreted with caution given Depth bands D1, D2 and D3 grouped together in the incomplete sampling of shallow stations (see clusters A1 and A2 (Figs. 5 and 6). Species sampling effort; Fig. 2). succession in this zone was very rapid and the rate ARTICLE IN PRESS

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Fig. 3. Distribution and relative abundance of bivalves in the Porcupine Seabight and on the Porcupine Abyssal Plain, showing the total range and the relative abundance of the species. Sledge data were used with OTSB data where no sledge data available. Species are: (1) Thyasira ferruginea, (2) Myonera atlantica, (3) Abra sp1, (4) Delectopecten vitreus, (5) Neilonella saliciensis, (6) Kelliella atlantica, (7) Chlamys sp1, (8) Chlamys sp2, (9) Cuspidaria obesa, (10) Limopsis minuta, (11) Yoldiella inconspicua, (12) Similipecten similis, (13) Abra profundorum, (14) Yoldiella jeffreysi, (15) Cardiomya costellata, (16) Limatula sp1, (17) Nuculoidea bushae, (18) Bathyarca nodulosa, (19) Tropidomya abbreviata, (20) Cyclopecten ambiannulatus, (21) Poromya tornata, (22) Bathyarca glacilis, (23) Thyasira sp1, (24) Thyasira eumyaria, (25) Lyonsiella subquadrata, (26) Malletia cuneata, (27) Yoldiella sp1, (28) Policordia cf gemma, (29) Cuspidaria atlantica, (30) Cardiomya knudseni, (31) Thyasira granulosa, (32) Pristigloma nitens, (33) Thyasira obsoleta, (34) Lyonsiella atlantica, (35) Bathypecten eucymatus, (36) Lyonsiella formosa, (37) Spinula subexcisa, (38) Idas cf argenteus, (39) Dacrydium ockelmanni, (40) Spinula ﬁlatovae, (41) Thyasira succisa succisa, (42) Parvamussium lucidum, (43) Thyasira equalis, (44) Deminucula atacellana, (45) Mysella sp1, (46) Thyasira inﬂata, (47) Axinodon sp1, (48) Protocuspidaria verityi, (49) Propamussium centobi, (50) Ledella pustulosa pustulosa, (51) Poromya granulata, (52) Rinoclama notabilis, (53) Malletia obtusa, (54) Spinula hilleri, (55) Nuculoma granulosa, (56)Thyasira ultima, (57) Parvamussium centobi, (58) Ledella pustulosa marshalli, (59) Yoldiella semistriata, (60) Ledella ultima, (61) Xylophaga sp1, (62) Thyasira pygamea, (63) Brevinucula verrilli, (64) Malletia cf abyssorum, (65) Limopsis tenella, (66) Edentaria similis, (67) Hyalopecten undatus, (68) Limatula sp2, (69) Neilonella whoii, (70) Verticordia cf triangularis, (71) Bathyarca inaequisculpta, (72) Cuspidaria circinata, (73) Silicula fragilis, (74) Nuculana sp1, (75) Halonympha sp1, (76) Ledella aberrata.

of species addition was high with a peak at 1800 m. A high percentage of species (20%) were restricted to this zone (e.g. Deminucula atacellana, Nuculoma granulosa, Thyasira ultima and Lyonsiella formosa). The 1900 m boundary marked a change in the rate of species succession (Fig. 4). Approximately 70% of species were added at or above this depth and very few species were added at depths greater than 1900 m untilabyssaldepths were reached. A lower bathyal zone was identiﬁed, spanning depths between 1900 and 2900 m. Four species are addedinthiszone:Ledella ultima which has a depth range of 1900–4900 m, Limopsis tenella with a range of 2600–4900 m, Hyalopecten undatus with a depth range of 2700–4100 m and Xylophaga sp1 which was restricted to a depth range of 2000–2500 m. Ten species were lost in this zone and the rate of species succession was gradual. Fig. 4. Cumulative addition and loss of species with depth from However, this area, particularly between 2100 and full data set. Turnover (addition plus loss) of species is also 2600 m, was poorly sampled (Fig. 2), which could plotted. account for the lack of addition of species. ARTICLE IN PRESS

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Fig. 5. Hierarchical cluster analysis of presence–absence combined data (sledge and OTSB), based on Sorenson similarity coefﬁcient.

Fig. 6. Non-metric multi-dimensional scaling plot for presence–absence combined data, based on Sorenson similarity coefﬁcient. Stations were grouped into 500 m depth bands labelled by letters: (D1) 500–999, (D2) 1000–1499, (D3) 1500–1999, (D4) 2000–2499, (D5) 2500–2999, (D6) 3000–3499, (D7) 3500–3999, (D8) 4000–4499, (D9) 4500–5000. Clusters A1, A2, B1, B2, C, D and E are shown.

An abyssalzone was suggested below 2900 m identiﬁed by a change in the rate of succession in the Seabight and extending out to the Abyssal (addition and loss), which was very rapid (Fig. 4). Plain (Figs. 5 and 6). This region was also Six species were added in this area and 26 were ARTICLE IN PRESS

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Fig. 7. Distribution of assemblages in the area of study. Stations were grouped into 500 m depth bands labelled by letters: (D1) 500–999, (D2) 1000–1499, (D3) 1500–1999, (D4) 2000–2499, (D5) 2500–2999, (D6) 3000–3499, (D7) 3500–3999, (D8) 4000–4499, (D9) 4500–5000. Clusters A1, A2, B1, B2, C, D and E are shown.

Fig. 9. Distribution of Propamussium centobi and Yoldiella inconspicua in the Porcupine Seabight and AbyssalPlain.

lost. There was, however, a transition zone between 2900 and 4100 m (see clusters A1, C, and some samples of B2; Figs. 5 and 6) where only three species, Neilonella saliciensis Verticordia cf triangularis and Cuspidaria circinata, were added. In this region there was a gap in the data set (3000–3500 m), which corresponded with very rough terrain (Rice et al., 1991; Fig. 2). This could account for the lack of species addition in the transition zone. Samples from the ‘‘truly’’ abyssal zone, represented mainly by clusters B (most of samples) and few samples of A1 and D (Figs. 5 and 6), were marked by the presence of abyssalspecies, i.e. Nuculana sp1, Ledella aberrata, Silicula fragilis, Cuspidaria circinata and Halonympha sp1, with very restricted depth ranges (but see S. fragilis). The upper limit of this zone (4000–4200 m) was Fig. 8. Distribution of Thyasira obsoleta, Policordia cf gemma characterized by the loss of 15 species, most of and Yoldiella sp1 in the Porcupine Seabight and AbyssalPlain. which had very broad depth ranges (43000 m). ARTICLE IN PRESS

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The characterization of this zone was, however, quite difﬁcult since it was poorly sampled. This is the area between the mouth of the Porcupine Seabight and the BENGAL sampling site on the Porcupine AbyssalPlain( Howell et al., 2002).

3.3. Diversity trends

There was a pattern of increasing diversity downslope from 500 to 1600 m, followed by a decrease to minimum values at about 2600 m. This drop in diversity was followed by an increase up to maximum values at 4100 m and then again, a fall to 4900 m (the lower depth limit in this study). Although there was a signiﬁcant trend with depth (r2=0.177; po0.05) (Fig. 10), it was rather weak and not well represented by a linear correlation.

4. Discussion

The faunalcomposition of bivalvesin the Porcupine Seabight and Porcupine AbyssalPlain area varied with depth, but this change was very gradual( Fig. 3). Most species occurred over broad Fig. 10. Change in diversity with depth, given as ES(50) values depth ranges and overlapped in their distributions. (expected number of species obtained from a sample of 50 individuals) for each sample depth. The solid line is the Diversity showed a unimodaltrend with a regression line (y=2.27À0.001xÀ17.86EÀ09x2; F=13.62; diversity maximum at 4100 m. po0.05; n=65) ﬁtted using standard least-squares techniques.

4.1. Bathymetric distribution Two species, Kelliella atlantica and Myonera Though boundaries of faunalrenewalwith atlantica, presented the broadest depth ranges depth were found changes were less obvious than (500–4900 m). Despite their similar total depth those found for other deep-sea invertebrates (e.g. ranges, the depths of maximum abundance of Rowe and Menzies, 1969; Billett, 1991; Rice these two species were distinct (Table 1). The two et al.,1990; Cartes and Sarda` , 1993; Howell species show different feeding characteristics: K. et al., 2002). Most species exhibited broad depth atlantica is a suspension feeder, whereas M. ranges, i.e. some ranges extending over more than atlantica is a carnivorous species (Allen and 3000 m (see Table 1; Fig. 3), in agreement with Morgan, 1981; Allen, 2001). In contrast, some previous studies on bivalves (e.g. Sanders and species with different totaldepth ranges occurred Grassle, 1971; Grassle and Maciolek, 1992; Allen at their maximum abundances at around the same and Sanders, 1996). Nevertheless, nearly all species depth (e.g. Brevinucula verrilli, Yoldiella sp1, examined in this study reached their highest levels Hyalopecten undatus and Edentaria simplis; Table of abundance over more restricted depth ranges of 1). Some of these species had similar feeding 200–300 m (see Fig. 3). In general, the depth range modes (Allen and Turner, 1974; Allen and over which a species was present at maximum Morgan, 1981; Allen and Sanders, 1996). abundance did not correspond with the centre of Although physical factors have been suggested its totaldepth range (see Table 1). as important regulators of the bathymetric ARTICLE IN PRESS

C. Olabarria / Deep-Sea Research I 52 (2005) 15–31 25 distribution of species (see Rowe and Menzies, other taxa in the same and adjacent areas (Gage, 1969; Haedrich et al., 1980), biological interactions 1986; Rice et al., 1990; Billett, 1991; Howell et al., seem to have an important role in governing the 2002). However, various studies have shown that ranges of distribution of many taxa (Rex, 1977, patterns of faunalchange vary considerably 1981; Cartes et al., 2003). The results of this study between taxa and geographic locations (Rex, suggest that the distribution of species, i.e. with a 1981; Billett, 1991; Gage and Tyler, 1991; Grassle totaldepth range over thousands of metres and and Maciolek, 1992; Cartes et al., 2003). In occurrence of maximum abundances over narrow general, the observed changes were very gradual depth ranges (o300 m), might be related to factors given that most species present had very broad operating at the local scale (e.g. food availability ranges of distribution. Species did undergo a and biological interactions) rather than global repeating sequentialchange with depth (see Fig. factors such as temperature or pressure. It is 3). Previous studies have also reported compara- possible, however, that temporal variability, i.e. tively low rates of zonation for bivalves (Sanders seasonaland/or interannualﬂuctuations, in abun- and Grassle, 1971; Rex, 1981; Allen and Sanders, dance of species might have affected the bathy- 1996). The pattern of species turnover, i.e. metric patterns observed in this study. Several appearance/disappearance, was very rapid down species such as Dacrydium ockelmanni, Delecto- to 1800 m and then more gradualat greater pecten vitreus, K. atlantica, Limopsis minuta and depths. A slow decline in the standing stock of Neilonella saliciensis showed peaks of abundances bivalves with depth might lead to this decrease in at certain depths between 1979 and 1982. Particu- the turnover rates with depth. larly, K. atlantica showed a dramatic increase in The distribution of samples following a ‘‘hor- densities between 1300 and 2700 m, attaining a izontalgradient’’ (see assemblages; Fig. 7) might maximum abundance of 840 ind 100 mÀ2 at be due to the fact that most of species with broad 2700 m in September 1979. These spatially bathymetric ranges had distributions skewed to localized changes in populations have been re- the opposite ends of their depth ranges (Fig. 3), i.e. ported in the same area (see Billett et al., 2001)and depths of maximum abundance varied along a may be related to higher availability of food input horizontalrange. Nevertheless, four bathymetric (Billett et al., 2001; Cartes et al., 2002). In deep-sea discontinuities, more or less clearly delimited, domains, peaks in recruitment and gametogenesis occurred: at 750, 1900, 2900 and 4100 m (see in macrofauna have been related to availability of Figs. 3–5). These boundaries translate to ﬁve food (e.g. Witte, 1996; Cartes et al., 2002; faunistic zones in this area. (1) A zone above Ramirez-Llodra et al., 2002). Short- and long- 750 m marked the change from shelf species to term changes in deep-sea populations have been bathyalspecies. (2) A zone from 750 to 1900 m attributed to seasonaland interannualvariation in corresponds to the upper and mid-bathyalzones food supply (e.g. Billett et al., 1983; Rice et al., taken together, where species turnover was rapid 1994; Danovaro et al., 1999; Billett et al., 2001). and diversity attained high values. The 1900 m Thus, the increase in abundances of adults and boundary was marked by changes in the rate of juveniles of these species between 1979 and 1982 species turnover and diversity. (3) A lower bathyal might be related to quality and/or quantity of food zone from 1900 to 2900 m was characterized by a supply rather than to localized stochastic popula- gradualrate of species succession and the addition tion variations. of only four species; many species reached their maximum abundances in the 2600–2800 m depth 4.2. Assemblages and patterns of zonation band. (4) A transition zone from 2900 to 4100 m was marked by a very rapid rate of succession and Although there were changes in the vertical a loss of about 35% of species; diversity reached distribution of bivalve assemblages in the Porcu- maximum values at 4100 m. In this region the pine Seabight and Porcupine AbyssalPlain,these bathyalfauna met and overlapped with the abyssal changes were not as strong as those reported for fauna. The 4100 m boundary marked the lower ARTICLE IN PRESS

26 C. Olabarria / Deep-Sea Research I 52 (2005) 15–31 limit of the distribution of many bathyal species. ture, currents, pressure, water masses), differences (5) The ‘‘truly’’ abyssal zone, from about in patterns of zonation have been related to 4100–4900 m (the lower depth limit of this study), biological factors such as the trophic level of the was characterized by the presence of abyssal taxon considered (Rex 1977, 1981; Cartes and species with restricted depth ranges and a few Carrasson, 2004) and life-history characteristics specimens of some bathyalspecies with very broad (Sanders and Grassle, 1971; Rex, 1981). distributions. The bathymetric distribution of fauna in the The patterns of zonation identified in this study Porcupine Seabight and adjacent AbyssalPlain departed, to an extent, from those identified in the has been related to diverse factors, although Porcupine Seabight by other workers (Billett 1991; hydrographic conditions have been invoked as Howell et al., 2002). However, the suggested being most important factors (Rice et al., 1990; boundaries at about 750, 1900 and 2900 m were Billett, 1991; Howell et al., 2002). For example, similar to those proposed for asteroids in the same Billett (1991) suggested that the main factors area (Howell et al., 2002). Similar boundaries have driving the holothurian zonation were physiologi- also been reported by other authors elsewhere. The calconstraints and hydrographic factors affecting boundary at 750 m was comparable with faunal the deposition and concentration of organic boundaries at 800–1000 m for echinoderms from matter. Howell et al. (2002) indicated the impor- the Rockall Trough (Gage, 1986), at 700–800 m tance of the permanent thermocline and water for fish species (Pearcy et al., 1982; Moranta et al., mass structure in determining the zonation pat- 1998) and megafauna (Hecker, 1990), at terns of seastars. Furthermore, Flach and Thom- 626–694 m for decapod crustaceans (Maynou sen (1998) indicated that physicaland chemical and Cartes, 2000), at 500 m for cerianthid factors such as flow velocities and organic matter anemones (Shepard et al., 1986), and at 530 m supply could be very important parameters struc- for protrobranch bivalves (Allen and Sanders, turing macrofauna. Although water mass structure 1996). The boundary at 1900 m has been and temperature might have an effect on the previously reported at 1900–2200 m for fish bathymetric distribution of bivalves in Porcupine species (Pearcy et al., 1982), echinoderms (Gage, Seabight (see detailed description of these physical 1986), megafauna (Hecker, 1990) and decapod factors in Howell et al., 2002), biological factors crustaceans (Cartes and Sarda` , 1993). The dis- could also play a more important role. The continuity observed at 2900 m is comparable to reduced strength of zonation shown by bivalves, that found at about 2800 m, i.e. abyssalrise, for compared to other faunistic groups in the Porcu- gastropods (Rex, 1977) and seastars (Howell et al., pine Seabight and adjacent AbyssalPlain( Rice et 2002). Finally, the boundary placed around al., 1990; Billett, 1991; Flach and Thomsen, 1998; 4100 m, i.e. the bathyalto abyssaltransition, Howell et al., 2002), has also been reported in might be comparable to a shallower boundary other studies elsewhere (e.g. Sanders and Grassle, (3300 m) found for megafauna in the Porcupine 1971; Rex, 1981; Allen and Sanders, 1996). Seabight (Billet, 1991; Howell et al., 2002). The bathymetric distribution of bivalves in the Causes of zonation in the deep sea are complex area of study could be explained by a combination and several factors, i.e. physical and/or biological, of biological and physical factors. In deep-sea may act together to produce the observed patterns. fauna, rates of zonation differ because of the Physicalfactors such as geologicaland topogra- biological interactions among species (Cartes and phicalfeatures, pressure, temperature, water Carrasson, 2004). In general, zonation rates masses structure or currents (e.g. Rowe and increase with trophic level (or size) (Rex, 1977; Menzies, 1969; Rex, 1977; Pearcy et al., 1982; Cartes and Carrasson, 2004). Thus, faunalrepla- Gage, 1986; Hecker, 1990; Cartes and Sarda` , 1993; cement with depth is more rapid among predators Abello´ et al., 2002) may play an important role in and croppers than infaunaldeposit-feeders such as patterns of zonation. Apart from the local hetero- polychaetes and bivalves (Rex, 1977). Although geneity in environmentalconditions (e.g. tempera- the mode of larval development and degree of ARTICLE IN PRESS

C. Olabarria / Deep-Sea Research I 52 (2005) 15–31 27 mobility have been reported as some of the causes materialoriginating in the water columnand on affecting the rate of species replacement (Sanders the continental shelf flows along the channels and Grassle, 1971; Haedrich et al., 1980; Allen and system in the Porcupine Seabight (Rice et al., Sanders, 1996; Cartes and Carrasson, 2004), recent 1991), and organic matter sinks along with studies have indicated that developmental mode is inorganic particulate matter. Amounts of organic not the only factor determining zonation and matter may be higher in the channelsystems than dispersaldistance (see Young et al., 1997). In fact, surrounding areas affecting the distribution of some of the most widespread species in deep sea species and assemblages in the Seabight (Figs. 3 present non-planktotrophic development and sev- and 7; Cartes et al., 2002). Furthermore, pulses of eralplanktotrophic species are confined to regions food arriving sporadically may tend to accumulate with high food availability (Young et al., 1997). in this channels system that acts as trap for Thus, other variables related with dispersal abil- sediments (see Gili et al., 2000). Thus, these ities such as egg size and fecundity should be taken fluctuations in food supply can generate a high into account to explain intensity of zonation variability in patterns of abundance and distribu- (Cartes and Carrasson, 2004). Despite the variation of species over time (see temporalvariability bility in reproductive patterns of deep-sea bivalves in Section 4.1). and echinoderms (seastars and holothurians) many of species present lecitotrophic development 4.3. Diversity (Billet, 1991; Gage and Tyler, 1991; Le Pennec and Beninger, 2000; Ramirez-Llodra et al., 2002). It is Diversity trends in the deep sea are very possible that bivalves present a higher dispersal variable. Various faunal groups have shown ability than echinoderms with the same type of different depth–diversity trends (e.g. Sanders and larval development. Therefore, the lower trophic Hessler, 1969; Rex, 1973, 1981; Carney and Carey, level and a higher dispersal ability of bivalves 1982; Cartes and Sarda` , 1992; Paterson and compared to seastars and holothurians might in Lambshead, 1995; Allen and Sanders, 1996; Rex part explain differences in rates of zonation among et al., 1997; Howell et al., 2002). However, this these groups. In contrast, sponges, which belong large variation might in part be a result of the to a low trophic level, i.e. suspension-feeders, and different collecting techniques and analytical present planktotrophic development (Witte, 1996), methods used for estimating diversity (Rex et al., were more heavily zoned than bivalves in the 1997). High diversity in the deep sea has been Porcupine Seabight (Rice et al., 1990). This attributed to environmental/or biologicalfactors distribution, however, seemed to be related to (see for review Stuart et al., 2003). specific hydrographic conditions in the area (Rice A number of studies have found that gastropods et al., 1990). and protobranchs show parabolic trends in diver- In addition, the hydrography and topographical sity, with peaks at upper rise depths features of the area may have a strong effect on (2000–3000 m) (Rex, 1981, 1983; Rex et al., patterns of species distribution (see Cartes et al., 1997). However, Allen and Sanders (1996) re- 2002). Porcupine Seabight presents an unusual ported different trends in the diversity of proto- canyon-like topography (see Section 2.1; Rice branchs from Atlantic basins, with diversity peaks et al., 1991). Sedimentation (organic and inorganic in deeper waters (3000–4000 m) followed by a fluxes) and hydrodynamics in submarine canyons drop to the deepest parts of the basins (5000 m). help to create special habitats characterized by Also, in most basins there was a dip in diversity high abundance, biomass and diversity of species between 2000 and 2600 m. In the Western (Vetter and Dayton, 1998; Gili et al., 2000; Cartes European basin, for example, diversity values et al., 2002). Organic matter contents have been were high with a diversity minimum at about reported to be higher in submarine canyons than 2500 m and a maximum at 4400 m. over the surrounding slope areas (Danovaro et al., In this study, diversity did follow a concave 1999; Gili et al., 2000; Cartes et al., 2002). Detrital unimodaltrend ( Fig. 10) similar to trends ARTICLE IN PRESS

28 C. Olabarria / Deep-Sea Research I 52 (2005) 15–31 previously shown for gastropods and bivalves Acknowledgements (Rex, 1981, 1983; Rex et al., 1997). This diversity pattern is similar to that found for seastars in the I would like to thank the officers and crews of Porcupine Seabight (Howell et al., 2002), although RSS Challenger and RSS Discovery, as well as the diversity of this group reached maximum values at colleagues who have been instrumental in collect- 1800 and 4700 m. Furthermore, the observed ing the samples used in this study. This research pattern matched that exhibited by protobranchs has been supported by a Marie Curie Fellowship from some Atlantic basins (Allen and Sanders, of the European Community programme ‘‘Energy, 1996). Nevertheless, diversity values were not as Environment and Sustainable Development’’ un- high as those found in the West European Basin der contract EVK2-CT-2001-50010 to Celia Ola- by the latter authors. barria. In addition, I would also like to thank Dr The low values of diversity between 2100 and M Rex, Dr B Bett and Dr D Billett for their 2700 m were due in part to the large numbers of valuable comments on the first draft of this individuals of Kelliella atlantica in some of the manuscript. I also thank the three anonymous samples collected at these depths. For example, referees whose comments improved considerably this species accounted for 93% of individuals the originalmanuscript. at 2650 m. The high values of diversity found at 4100 m were due to the large number of species recorded at this depth (16–20 species References per sample). Between 4800 and 4900 m, diversity values dropped since the number of species Abello´ , P., Carbonell, A., Torres, P., 2002. Biogeography of per sample was lower (4–9 species per sample). epibenthic crustaceans on the shelf and upper slope off the These results indicate high values of diversity Iberian Peninsula Mediterranean coasts: implications for at abyssaldepths. Rex et al. (2005) proposed the establishment of natural management areas. Scientia the ‘‘source-sink hypothesis for abyssalbiodiver- Marina 66, 183–198. Allen, J.A., 1998. The deep-water species of Dacrydium Torell, sity’’ suggesting that abyssalpopulationsmight 1859 (Dacrydiinae: Mytilidae: Bivalvia), of the Atlantic. be maintained by immigration from adjacent Malacologia 1–2, 1–36. bathyalpopulationsof species with high dispersal Allen, J.A., 2001. The family Kelliellidae (Bivalvia: Hetero- ability. If so, this hypothesis, together with the donta) from the deep Atlantic and its relationship with the low impact of predation on bivalve species at family Vesicomyidae. Zoological Journal of the Linnean Society 131, 199–226. these depths (Allen and Sanders, 1996), could Allen, J.A., Hannah, F.J., 1989. Studies on the deep-sea explain in part the high diversity values found Protobranchia. The subfamily Ledellinae (Nuculanidae). at 4100 m. Furthermore, severalstudies reported Bulletin of the British Museum (Natural History). Zoology strong fluxes of organic matter to the Porcupine 55, 123–171. AbyssalPlain(e.g. Thurston et al., 1998; Billett Allen, J.A., Morgan, R., 1981. The functional morphology of the families Cuspidariidae and Poromyidae et al., 2001; Fabiano et al., 2001). Although (Mollusca: Bivalvia) of the abyssal Atlantic. Philosophical seasonally variable, this supply of organic Transactions of the RoyalSociety of London B 291, matter at abyssaldepths might be responsible 413–546. for the increase of diversity observed at 4100 m. Allen, J.A., Sanders, H.L., 1996. The zoogeography, diversity For instance, some trophic groups such as deposit- and origin of the deep-sea protobranch bivalves of the Atlantic: the epilogue. Progress in Oceanography 38, and suspension-feeders would be favoured by 95–153. this food supply. In fact, Thurston et al. Allen, J.A., Turner, J.F., 1974. On the functional morphology (1998) and Billett et al. (2001) found that of the family Verticordiidae (Bivalvia) with descriptions of particle fluxes arriving at the sea floor on the new species from the abyssal Atlantic. Philosophical Porcupine AbyssalPlainwere very important Transactions of the RoyalSociety of London B 268, 401–536. in determining changes in the specific com- Bett, B.J., 2001. UK Atlantic margin environmental survey: position and abundance of megafaunalassem- introduction and overview of bathyalbenthic ecology. blages. ContinentalShelfResearch 21, 917–956. ARTICLE IN PRESS

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