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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 Olabarria
Southampton Oceanography Centre, DEEPSEAS Benthic Biology Group, Empress Dock, Southampton SO14 3ZH, UK
Received 23 April 2004; 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 midbathyal zones taken together; (3) a lower bathyal zone 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 bathyal species 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
Departamento de Ecoloxı́a e Bioloxı́a Animal, Area Ecologı́a, 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).
0967-0637/$ - see front matter r 2004 Elsevier Ltd. All rights reserved.
doi:10.1016/j.dsr.2004.09.005
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C. Olabarria / Deep-Sea Research I 52 (2005) 15–31
1. Introduction
Although zonation of fauna, i.e. change of
species composition with depth, in the deep sea
have been broadly documented (see Howell et al.,
2002), most studies have dealt only with the
megafauna (see Cartes et al., 2003; Cartes and
Carrasson, 2004). Different faunal zones, i.e.
regions of lesser faunal change bounded by regions
of greater faunal change, have been proposed in
the deep sea, but there is still some disagreement
over the terminology of these zones (see for review
Howell et al., 2002) and their bathymetric limits.
Faunal boundaries reported in the literature
vary depending on the taxonomic group considered (e.g. Vinogradova et al., 1959; Rowe
and Menzies, 1969; Rex, 1973, 1981; Gage et al.,
1985; Billett, 1991; Howell et al., 2002). Faunal
zonation appears to be more apparent in higher
trophic levels, e.g. fish and crustaceans, than in
lower trophic levels, such as polychaetes or
bivalves (see Cartes et al., 2003; Cartes and
Carrasson, 2004).
Many of the previous studies focused on general
faunal zonation patterns (e.g. Rowe and Menzies,
1969; Ohta, 1983), or on the zonation of specific
taxonomic groups (e.g. Rex, 1977; Southward,
1979; Carney and Carey, 1982; Gage, 1986;
Billett, 1991; Cartes and Sardà, 1993; Howell et
al., 2002). Such studies have revealed that there is
replacement of species with depth and that most of
the species show restricted depth ranges (e.g.
Murray, 1895; Rex, 1977; Carney et al., 1983;
Etter and Rex, 1990; Howell et al., 2002). Causes
of this zonation have been attributed to physical
and/or biological factors such as temperature
(Rowe and Menzies, 1969), pressure (Young et
al., 1996), hydrographic conditions and topography (Lampitt et al., 1986; Rice et al., 1990),
nutrient input (Rex, 1981; Rice et al., 1990),
larval dispersal (Rowe and Menzies, 1969;
Billett 1991), competition, predation and trophic
level (Rex, 1977, 1981; Cartes and Sardà,
1993). Nevertheless, the causes for the change in
species composition with depth are complex
and several factors might act to produce the
observed pattern. Therefore, detailed studies of
bathymetric distribution of deep-sea organisms
may help to elucidate the factors driving these
patterns.
In the Porcupine Seabight and adjacent areas
diverse zones of faunal change have been consistently reported. In general, though with important
local variations, a first boundary related to the
water mass structure and permanent thermocline
occurs at 700 m depth (e.g. Gage, 1986; Howell
et al., 2002). A second faunal turnover associated
with changes in currents occurs at 1100 m
(Howell et al., 2002). In addition, there is a third
boundary at about 1700 m marked by a rapid
faunal change and related to changes in temperature and water masses (Gage, 1986; Billett, 1991;
Howell et al., 2002). Finally, there is a boundary at
3000 m that separates bathyal and abyssal fauna
(Lampitt et al., 1986; Billett, 1991; Howell et al.,
2002). This zonation scheme is based on studies of
megafaunal groups, whereas smaller macrofauna
has been generally neglected. Studies focusing on
macrofaunal assemblages belonging to lower
trophic levels, e.g. polychaetes, gastropods or
bivalves, could contribute to a better understanding of the structure of deep-sea communities in this
area.
Bivalves represent about 10% of the deep-sea
macrobenthic fauna, being the third taxon in
abundance after polychaetes and peracarid crustaceans (Allen and Sanders 1996). Deep-sea
bivalves have been studied largely from a faunistic
and taxonomic point of view (e.g. Knudsen,
1970; Sanders and Allen, 1973; Allen and
Turner, 1974; Allen and Morgan, 1981; Allen
and Hannah, 1989; Allen 1998). Studies on
the diversity patterns of deep-sea bivalves have
been also reported from a number of areas (e.g.
Rex, 1981; Grassle and Maciolek, 1992; Rex et al.,
1993, 1997, 2000; Allen and Sanders, 1996).
Nevertheless, few studies have investigated patterns of bathymetric distribution and zonation of
bivalves in detail (but see Allen and Sanders,
1996).
This study, based on a large data set, examines
the bathymetric distribution of bivalves from the
Porcupine Seabight and adjacent Abyssal Plain
(NE Atlantic), patterns of zonation and diversity–depth trends. Possible causes of these patterns
are also discussed.
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2. Material and methods
2.1. Study area
The Porcupine Seabight and Porcupine Abyssal
Plain are located more than 200 km to the southwest of Ireland (Fig. 1). The Porcupine Seabight is
an amphitheatre-shaped embayment in the continental margin to the southwest of Ireland, and its
sides slope steadily from the edge of the Irish Shelf
at 200 m down to a depth of about 4000 m (site
described in Rice et al., 1991). The Seabight opens
onto the Porcupine Abyssal Plain through a
relatively narrow entrance to the southwest (Rice
et al., 1991). The Porcupine Abyssal Plain lies
south of the Rockall Trough and north of the
Iberian Abyssal Plain, at a depth between 4000
and 5000 m. The Seabight is bound on its west and
northwest side by the Porcupine Bank and on its
south and southeast side by the Goban Spur,
leaving a narrow entrance. The western slopes of
the Porcupine Seabight are steeper than the
eastern slopes. The eastern slope of the Seabight
differs markedly from the western one because of
the presence of many channels, which coalesce to
form a single large channel or canyon running
through the Seabight. The channels are still areas
of active transport where large amounts of detrital
Fig. 1. Location of the study area and sampling stations.
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material are accumulated. No sediment fan is
evident where the channel opens onto the Abyssal
Plain, indicating either little detrital material is
transported or that such material is distributed
once it reaches the Abyssal Plain (Rice et al.,
1991).
2.2. Collection and treatment of samples
A total of 76 epibenthic sledge and 50 otter
trawl samples was collected between 500 and
4866 m over a period of 22 years. These samples
were taken during the Institute of Oceanographic
Sciences (IOS) biology programme in the Porcupine Seabight and adjacent Abyssal Plain between
November 1977 and December 1986 (Rice
et al., 1991) and during the BENGAL programme
on the Porcupine Abyssal Plain between September 1995 and October 1998 (Billett and Rice,
2001). Despite this extensive sampling programme,
there were several gaps in the data set (Fig. 2)
that might affect the outcome of this study.
Nevertheless, many depth bands were represented
by more than 3 sampling runs (sledge and
OTSB), so data were reliable and produced a
quite comprehensive representation of species
distribution.
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 trawl doors to
provide better estimates of the length of the tow.
Mercury tilt switches in this monitor indicate the
arrival and 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
faunal group 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
infauna. Despite the shortcomings, samples collected
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C. Olabarria / Deep-Sea Research I 52 (2005) 15–31
2.3. Data treatment
Fig. 2. Distribution of (A) sledge, (B) OTSB sampling effort in
the Porcupine Seabight and Abyssal Plain in 100 m depth
bands. Grey bars: total number of samples collected in that
particular depth band; black bars: samples containing bivalves.
in this area over this long period of time provided an
important data set in order to get better understanding of patterns of distribution of species and
processes driving these patterns in the northeast
Atlantic Ocean.
Samples were sorted on deck and fixed in boraxbuffered 4% formaldehyde in seawater and then
preserved in 80% alcohol. Specimens were identified to species level when possible. A total of
131,334 individuals belonging to 76 species were
collected. The number of species in each sample
was determined per sample and numerical density
was standardized to 100 m2.
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
faunal turnover occurs, i.e. zonation patterns.
To identify the main assemblages, both sledge
and trawl data 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
depth bands and labelled D1–D9. This grouping
allowed the data to be investigated in terms of
depth rather than species change (see Howell et al.,
2002). The Sorenson similarity coefficient (Clarke
and Warwick, 1994) was applied to the transformed grouped data to obtain a similarity matrix.
Subsequently, hierarchical clustering with groupaveraged linking and non-metric multi-dimensional scaling using the similarity matrix were
performed. To test the relationship between depth
and change in species composition a Spearman’s
rank correlation coefficient was calculated for the
x-ordinate of the MDS plot and depth.
Diversity was analysed with the rarefaction
method (Hurlbert, 1971). Values for the expected
number of species in a sample of 50 individuals
were extracted from the programme PRIMER
(Plymouth Routines in Multivariate Ecological
Research, ver. 5), and a graph of expected number
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of species against depth was plotted. The ES (50)
value was used in this study because of the patchy
distributions of species and low abundances of
many of them. Sledge and OTSB data were
combined after separate analyses indicated similar
results from both gears individually.
3. Results
3.1. Species distribution
In general, most of species showed a broad
depth range with some species’ ranges extended
over more than 3000 m (e.g. Pristigloma nitens,
Thyasira equalis, Kelliella atlantica, Abra profundorum and Cuspidaria obesa; Table 1, Fig. 3).
Although there was a very gradual replacement of
species with depth (Fig. 3) many species overlapped in their depth ranges, i.e. approximately
62% of species coexisted in the 2600–3000 m depth
range. A high percentage (67%) of species
occurred deeper than 3000 m, whereas 21% of
species occurred shallower than 2000 m (Table 1).
Only sixteen species showed comparatively narrow
depth ranges (o300 m) (Table 1) and most of them
occurred shallower than 1700 m (but see Nuculana sp1, Ledella aberrata, C. circinata, Halonympha sp1, Edentaria similis; Table 1). Despite most
species having broad bathymetric ranges, some
zones of enhanced species turnover were identified
(Fig. 4).
Most of species showed a patchy distribution
through their depth range, often occurring, in any
great abundance, only over a very narrow depth
range of 100–300 m (Fig. 3). The narrow depth of
greater abundance did not generally occur in the
middle of their total depth ranges (Table 1; Fig. 3).
For example, species such as Bathypecten eucymatus, Similipecten similis, Parvamussium permirum,
A. profundorum, L. ultima and Cardiomya knudseni
reached their respective relative high levels of
abundance at the start or end of their depth
ranges. In contrast, few species (e.g. Malletia cf
abyssorum, Verticordia cf triangularis, Yoldiella
sp1, K. atlantica) presented their maximum
abundances in the middle of their total depth
ranges.
19
Furthermore, various species co-occurred at
their maximum abundances at a particular depth
(see 2700–2800 m depth band; Table 1). Although
some species’ vertical ranges were broad, their
relative abundance patterns changed markedly
below 2500 m. For example, Ledella pustulosa
marshalli, Malletia obtusa and K. atlantica were
more abundant below this depth (Fig. 2), whereas
P. lucidum and Limatula sp1. decreased in
abundance.
Faunal discontinuities occurred at 2000–
2500 m and 3100–3500 m. Very few species were
present, and none occurred in large numbers (but
see Idas cf argenteus and Xylophaga sp1). These
depths correspond to gaps in the data set (Rice et
al., 1991; Howell et al., 2001) and a rocky area
(3000–3500 m) at the base of the continental
slope.
3.2. Assemblages and patterns of zonation
Both Hierarchical Cluster Analysis and MDS
evidenced an arrangement of stations in 5 different
groups (Figs. 5 and 6). These groups (A, B, C, D
and E; Fig. 5) were very dissimilar to each other
(similarity close to zero). Although a Spearman’s
rank correlation of depth with the MDS-ordinate
gave a significant result (0.64; po0.0001), some
samples from different depths were grouped
together (for example, group A). Despite the
arrangement of the stations according to a depth
gradient there was also some indication of
alongslope organization within area of study (see
assemblages; Fig. 7). Most species with broad
bathymetric ranges were widespread in the area
(e.g. Thyasira obsoleta, Polycordia gemma, Yoldiella sp1; Fig. 8); however, a few species showed
more restricted horizontal distributions (e.g. Propamussium centobi, Yoldiella inconspicua; Fig. 9).
Nevertheless, four more or less clearly delimited
bathymetric boundaries could be found. An upper
slope zone from 500 to 750 m could be identified
by both cluster and MDS analysis (cluster E, Figs.
5 and 6). The rate of species succession was
gradual in this region with an addition of 8 species
that extended throughout the area and beyond
(but see Chlamys sp2) (Fig. 3). Two species typified this zone, Chlamys sp1 and Chlamys sp2.
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Table 1
The depth distribution of bivalve species from the Porcupine Seabight and the Porcupine Abyssal Plain
Species
Depth range
(m)
Depth of maximum
abundance (m)
Species
Depth range
(m)
Depth of maximum
abundance (m)
Deminucula atacellana d
Nuculoidea bushae d
Brevinucula verrilli d
Nuculoma granulosa d
Pristigloma nitens d
Nuculana sp1 d *
Ledella aberrata d
Ledella pustulosa
marshalli d
Ledella pustulosa
pustulosa d
Ledella ultima d
Spinula filatovae d
Spinula hilleri d
Spinula subexcisa d
Silicula fragilis d
Malletia cf abyssorum d
Malletia cuneata d
Malletia obtusa d
Neilonella whoii d
Neilonella saliciensis d
Yoldiella sp1 d
Yoldiella inconspicua d
Yoldiella jeffreysi d
Yoldiella semistriata d
Bathyarca glacilis *
Bathyarca inaequisculpta
Bathyarca nodulosa *
Limopsis minuta
Limopsis tenella
Dacrydium ockelmanni s
Idas cf argenteus s
Chlamys sp1 * s
Chlamys sp2 s
Cyclopecten
ambiannulatus s
Delectopecten vitreus s
Hyalopecten undatus s
Bathypecten eucymatus s
Similipecten similis s
Parvamusium lucidum s
1200–1800
700–2900
2600–4100
1600–1700
900–4000
4800–4900
4800–4900
1600–4100
1200–1400
900–1000
2700–2800
1600–1700
2600–2700
4800–4900
4800–4900
2700–2800
Parvamussium permirum
Propamussium centobi
Limatula sp1
Limatula sp2
Axinodon sp1
Thyasira equalis d
Thyasira eumyaria d
Thyasira ferruginea d
1600–4900
1300–4900
700–2800
2700–4900
1200–3600
1200–4900
900–1500
500–2700
1600–1700
2700–2800
1100–1200
3900–4000
1200–1300
1200–1300
900–1000
500–600
1300–2700
1600–1700
Thyasira granulosa
900–1000
900–1000
1900–4900
1100–4100
1400–4100
1100–3600
4000–4900
2600–4900
900–4900
1400–4000
3000–4900
500–4000
900–4900
700–4000
700–4000
1600–2000
900–1000
3500–4900
800–900
600–1700
2600–4900
1100–4900
1100–3700
500–900
500–700
800–4900
4800–4900
1300–1400
2700–2800
1100–1200
4800–4900
3900–4000
4000–4100
3900–4000
3000–3100
2600–2700
2700–2800
700–800
1400–1500
1900–2000
900–1000
3900–4000
800–900
1300–1400
2700–2800
1600–1700
2400–2500
700–800
600–700
3900–4000
Thyasira inflata d
Thyasira obsoleta d
Thyasira pygmaea d
Thyasira sp1 d
Thyasira succisa succisa d
Thyasira ultima d
Kelliella atlantica s
Mysella sp1
Abra profundorum * d
Abra sp1 d
Xylophaga sp1
Lyonsiella abyssicola c
Lyonsiella formosa c
Lyonsiella subquadrata c
Verticordia cf triangularis c
Policordia cf gemma * c
Cuspidaria atlantica c
Cuspidaria circinata c
Cuspidaria obesa c
Cardiomya costellata * c
Cardiomya knudseni * c
Myonera atlantica c
Rhinoclama notabilis c
Tropidomya abbreviata * c
1200–3600
900–4100
2600–2700
900–2800
1100–3600
1600–1700
500–4900
1200–3100
700–4900
500–1300
2000–2500
1100–1400
1100–1700
900–2800
3000–4400
900–4900
900–4100
4000–4100
600–4900
700–1400
900–4000
500–4900
1400–4600
800–900
2600–2700
1200–1300
2600–2700
900–1000
1900–2000
1600–1700
2600–2700
1300–1400
700–800
500–600
2000–2100
1100–1200
1100–1200
1200–1300
3500–3600
1100–1200
3500–3600
4000–4100
1100–1200
1300–1400
3900–4000
1300–1400
4000–4100
800–900
500–4100
2700–4100
1100–4000
700–3700
1100–3600
1200–1300
2700–2800
1100–1200
700–800
1600–1700
Halonympha sp1 * c
Protocuspidaria verityi
Edentaria simplis c
Poromya granulata c
Poromya tornata c
4800–4900
1300–4900
2700–2800
1300–3700
800–4900
4800–4900
2700–2800
2700–2800
1300–1400
3900–4000
d
c
*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
750 m should be interpreted with caution given
the incomplete sampling of shallow stations (see
sampling effort; Fig. 2).
A bathyal zone extended from 750 to 1900 m.
Depth bands D1, D2 and D3 grouped together in
clusters A1 and A2 (Figs. 5 and 6). Species
succession in this zone was very rapid and the rate
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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.
Fig. 4. Cumulative addition and loss of species with depth from
full data set. Turnover (addition plus loss) of species is also
plotted.
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
until abyssal depths were reached.
A lower bathyal zone was identified, spanning
depths between 1900 and 2900 m. Four species are
added in this zone: 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.
However, this area, particularly between 2100 and
2600 m, was poorly sampled (Fig. 2), which could
account for the lack of addition of species.
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C. Olabarria / Deep-Sea Research I 52 (2005) 15–31
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 abyssal zone was suggested below 2900 m
in the Seabight and extending out to the Abyssal
Plain (Figs. 5 and 6). This region was also
identified by a change in the rate of succession
(addition and loss), which was very rapid (Fig. 4).
Six species were added in this area and 26 were
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C. Olabarria / Deep-Sea Research I 52 (2005) 15–31
23
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 Abyssal Plain.
Fig. 8. Distribution of Thyasira obsoleta, Policordia cf gemma
and Yoldiella sp1 in the Porcupine Seabight and Abyssal Plain.
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 abyssal species, 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
characterized by the loss of 15 species, most of
which had very broad depth ranges (43000 m).
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C. Olabarria / Deep-Sea Research I 52 (2005) 15–31
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 Abyssal Plain (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 faunal composition of bivalves in the
Porcupine Seabight and Porcupine Abyssal Plain
area varied with depth, but this change was very
gradual (Fig. 3). Most species occurred over broad
depth ranges and overlapped in their distributions.
Diversity showed a unimodal trend with a
diversity maximum at 4100 m.
Fig. 10. Change in diversity with depth, given as ES(50) values
(expected number of species obtained from a sample of 50
individuals) for each sample depth. The solid line is the
regression line (y=2.27 0.001x 17.86E 09x2; F=13.62;
po0.05; n=65) fitted using standard least-squares techniques.
4.1. Bathymetric distribution
Though boundaries of faunal renewal with
depth were found changes were less obvious than
those found for other deep-sea invertebrates (e.g.
Rowe and Menzies, 1969; Billett, 1991; Rice
et al.,1990; Cartes and Sardà, 1993; Howell
et al., 2002). Most species exhibited broad depth
ranges, i.e. some ranges extending over more than
3000 m (see Table 1; Fig. 3), in agreement with
previous studies on bivalves (e.g. Sanders and
Grassle, 1971; Grassle and Maciolek, 1992; Allen
and Sanders, 1996). Nevertheless, nearly all species
examined in this study reached their highest levels
of abundance over more restricted depth ranges of
200–300 m (see Fig. 3). In general, the depth range
over which a species was present at maximum
abundance did not correspond with the centre of
its total depth range (see Table 1).
Two species, Kelliella atlantica and Myonera
atlantica, presented the broadest depth ranges
(500–4900 m). Despite their similar total depth
ranges, the depths of maximum abundance of
these two species were distinct (Table 1). The two
species show different feeding characteristics: K.
atlantica is a suspension feeder, whereas M.
atlantica is a carnivorous species (Allen and
Morgan, 1981; Allen, 2001). In contrast, some
species with different total depth ranges occurred
at their maximum abundances at around the same
depth (e.g. Brevinucula verrilli, Yoldiella sp1,
Hyalopecten undatus and Edentaria simplis; Table
1). Some of these species had similar feeding
modes (Allen and Turner, 1974; Allen and
Morgan, 1981; Allen and Sanders, 1996).
Although physical factors have been suggested
as important regulators of the bathymetric
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C. Olabarria / Deep-Sea Research I 52 (2005) 15–31
distribution of species (see Rowe and Menzies,
1969; Haedrich et al., 1980), biological interactions
seem to have an important role in governing the
ranges of distribution of many taxa (Rex, 1977,
1981; Cartes et al., 2003). The results of this study
suggest that the distribution of species, i.e. with a
total depth range over thousands of metres and
occurrence of maximum abundances over narrow
depth ranges (o300 m), might be related to factors
operating at the local scale (e.g. food availability
and biological interactions) rather than global
factors such as temperature or pressure. It is
possible, however, that temporal variability, i.e.
seasonal and/or interannual fluctuations, in abundance of species might have affected the bathymetric patterns observed in this study. Several
species such as Dacrydium ockelmanni, Delectopecten vitreus, K. atlantica, Limopsis minuta and
Neilonella saliciensis showed peaks of abundances
at certain depths between 1979 and 1982. Particularly, K. atlantica showed a dramatic increase in
densities between 1300 and 2700 m, attaining a
maximum abundance of 840 ind 100 m 2 at
2700 m in September 1979. These spatially
localized changes in populations have been reported in the same area (see Billett et al., 2001) and
may be related to higher availability of food input
(Billett et al., 2001; Cartes et al., 2002). In deep-sea
domains, peaks in recruitment and gametogenesis
in macrofauna have been related to availability of
food (e.g. Witte, 1996; Cartes et al., 2002;
Ramirez-Llodra et al., 2002). Short- and longterm changes in deep-sea populations have been
attributed to seasonal and interannual variation in
food supply (e.g. Billett et al., 1983; Rice et al.,
1994; Danovaro et al., 1999; Billett et al., 2001).
Thus, the increase in abundances of adults and
juveniles of these species between 1979 and 1982
might be related to quality and/or quantity of food
supply rather than to localized stochastic population variations.
4.2. Assemblages and patterns of zonation
Although there were changes in the vertical
distribution of bivalve assemblages in the Porcupine Seabight and Porcupine Abyssal Plain, these
changes were not as strong as those reported for
25
other taxa in the same and adjacent areas (Gage,
1986; Rice et al., 1990; Billett, 1991; Howell et al.,
2002). However, various studies have shown that
patterns of faunal change vary considerably
between taxa and geographic locations (Rex,
1981; Billett, 1991; Gage and Tyler, 1991; Grassle
and Maciolek, 1992; Cartes et al., 2003). In
general, the observed changes were very gradual
given that most species present had very broad
ranges of distribution. Species did undergo a
repeating sequential change with depth (see Fig.
3). Previous studies have also reported comparatively low rates of zonation for bivalves (Sanders
and Grassle, 1971; Rex, 1981; Allen and Sanders,
1996). The pattern of species turnover, i.e.
appearance/disappearance, was very rapid down
to 1800 m and then more gradual at greater
depths. A slow decline in the standing stock of
bivalves with depth might lead to this decrease in
the turnover rates with depth.
The distribution of samples following a ‘‘horizontal gradient’’ (see assemblages; Fig. 7) might
be due to the fact that most of species with broad
bathymetric ranges had distributions skewed to
the opposite ends of their depth ranges (Fig. 3), i.e.
depths of maximum abundance varied along a
horizontal range. Nevertheless, four bathymetric
discontinuities, more or less clearly delimited,
occurred: at 750, 1900, 2900 and 4100 m (see
Figs. 3–5). These boundaries translate to five
faunistic zones in this area. (1) A zone above
750 m marked the change from shelf species to
bathyal species. (2) A zone from 750 to 1900 m
corresponds to the upper and mid-bathyal zones
taken together, where species turnover was rapid
and diversity attained high values. The 1900 m
boundary was marked by changes in the rate of
species turnover and diversity. (3) A lower bathyal
zone from 1900 to 2900 m was characterized by a
gradual rate of species succession and the addition
of only four species; many species reached their
maximum abundances in the 2600–2800 m depth
band. (4) A transition zone from 2900 to 4100 m
was marked by a very rapid rate of succession and
a loss of about 35% of species; diversity reached
maximum values at 4100 m. In this region the
bathyal fauna met and overlapped with the abyssal
fauna. The 4100 m boundary marked the lower
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26
C. Olabarria / Deep-Sea Research I 52 (2005) 15–31
limit of the distribution of many bathyal species.
(5) The ‘‘truly’’ abyssal zone, from about
4100–4900 m (the lower depth limit of this study),
was characterized by the presence of abyssal
species with restricted depth ranges and a few
specimens of some bathyal species with very broad
distributions.
The patterns of zonation identified in this study
departed, to an extent, from those identified in the
Porcupine Seabight by other workers (Billett 1991;
Howell et al., 2002). However, the suggested
boundaries at about 750, 1900 and 2900 m were
similar to those proposed for asteroids in the same
area (Howell et al., 2002). Similar boundaries have
also been reported by other authors elsewhere. The
boundary at 750 m was comparable with faunal
boundaries at 800–1000 m for echinoderms from
the Rockall Trough (Gage, 1986), at 700–800 m
for fish species (Pearcy et al., 1982; Moranta et al.,
1998) and megafauna (Hecker, 1990), at
626–694 m for decapod crustaceans (Maynou
and Cartes, 2000), at 500 m for cerianthid
anemones (Shepard et al., 1986), and at 530 m
for protrobranch bivalves (Allen and Sanders,
1996). The boundary at 1900 m has been
previously reported at 1900–2200 m for fish
species (Pearcy et al., 1982), echinoderms (Gage,
1986), megafauna (Hecker, 1990) and decapod
crustaceans (Cartes and Sardà, 1993). The discontinuity observed at 2900 m is comparable to
that found at about 2800 m, i.e. abyssal rise, for
gastropods (Rex, 1977) and seastars (Howell et al.,
2002). Finally, the boundary placed around
4100 m, i.e. the bathyal to abyssal transition,
might be comparable to a shallower boundary
(3300 m) found for megafauna in the Porcupine
Seabight (Billet, 1991; Howell et al., 2002).
Causes of zonation in the deep sea are complex
and several factors, i.e. physical and/or biological,
may act together to produce the observed patterns.
Physical factors such as geological and topographical features, pressure, temperature, water
masses structure or currents (e.g. Rowe and
Menzies, 1969; Rex, 1977; Pearcy et al., 1982;
Gage, 1986; Hecker, 1990; Cartes and Sardà, 1993;
Abelló et al., 2002) may play an important role in
patterns of zonation. Apart from the local heterogeneity in environmental conditions (e.g. tempera-
ture, currents, pressure, water masses), differences
in patterns of zonation have been related to
biological factors such as the trophic level of the
taxon considered (Rex 1977, 1981; Cartes and
Carrasson, 2004) and life-history characteristics
(Sanders and Grassle, 1971; Rex, 1981).
The bathymetric distribution of fauna in the
Porcupine Seabight and adjacent Abyssal Plain
has been related to diverse factors, although
hydrographic conditions have been invoked as
being most important factors (Rice et al., 1990;
Billett, 1991; Howell et al., 2002). For example,
Billett (1991) suggested that the main factors
driving the holothurian zonation were physiological constraints and hydrographic factors affecting
the deposition and concentration of organic
matter. Howell et al. (2002) indicated the importance of the permanent thermocline and water
mass structure in determining the zonation patterns of seastars. Furthermore, Flach and Thomsen (1998) indicated that physical and chemical
factors such as flow velocities and organic matter
supply could be very important parameters structuring macrofauna. Although water mass structure
and temperature might have an effect on the
bathymetric distribution of bivalves in Porcupine
Seabight (see detailed description of these physical
factors in Howell et al., 2002), biological factors
could also play a more important role. The
reduced strength of zonation shown by bivalves,
compared to other faunistic groups in the Porcupine Seabight and adjacent Abyssal Plain (Rice et
al., 1990; Billett, 1991; Flach and Thomsen, 1998;
Howell et al., 2002), has also been reported in
other studies elsewhere (e.g. Sanders and Grassle,
1971; Rex, 1981; Allen and Sanders, 1996).
The bathymetric distribution of bivalves in the
area of study could be explained by a combination
of biological and physical factors. In deep-sea
fauna, rates of zonation differ because of the
biological interactions among species (Cartes and
Carrasson, 2004). In general, zonation rates
increase with trophic level (or size) (Rex, 1977;
Cartes and Carrasson, 2004). Thus, faunal replacement with depth is more rapid among predators
and croppers than infaunal deposit-feeders such as
polychaetes and bivalves (Rex, 1977). Although
the mode of larval development and degree of
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C. Olabarria / Deep-Sea Research I 52 (2005) 15–31
mobility have been reported as some of the causes
affecting the rate of species replacement (Sanders
and Grassle, 1971; Haedrich et al., 1980; Allen and
Sanders, 1996; Cartes and Carrasson, 2004), recent
studies have indicated that developmental mode is
not the only factor determining zonation and
dispersal distance (see Young et al., 1997). In fact,
some of the most widespread species in deep sea
present non-planktotrophic development and several planktotrophic species are confined to regions
with high food availability (Young et al., 1997).
Thus, other variables related with dispersal abilities such as egg size and fecundity should be taken
into account to explain intensity of zonation
(Cartes and Carrasson, 2004). Despite the variability in reproductive patterns of deep-sea bivalves
and echinoderms (seastars and holothurians)
many of species present lecitotrophic development
(Billet, 1991; Gage and Tyler, 1991; Le Pennec and
Beninger, 2000; Ramirez-Llodra et al., 2002). It is
possible that bivalves present a higher dispersal
ability than echinoderms with the same type of
larval development. Therefore, the lower trophic
level and a higher dispersal ability of bivalves
compared to seastars and holothurians might in
part explain differences in rates of zonation among
these groups. In contrast, sponges, which belong
to a low trophic level, i.e. suspension-feeders, and
present planktotrophic development (Witte, 1996),
were more heavily zoned than bivalves in the
Porcupine Seabight (Rice et al., 1990). This
distribution, however, seemed to be related to
specific hydrographic conditions in the area (Rice
et al., 1990).
In addition, the hydrography and topographical
features of the area may have a strong effect on
patterns of species distribution (see Cartes et al.,
2002). Porcupine Seabight presents an unusual
canyon-like topography (see Section 2.1; Rice
et al., 1991). Sedimentation (organic and inorganic
fluxes) and hydrodynamics in submarine canyons
help to create special habitats characterized by
high abundance, biomass and diversity of species
(Vetter and Dayton, 1998; Gili et al., 2000; Cartes
et al., 2002). Organic matter contents have been
reported to be higher in submarine canyons than
over the surrounding slope areas (Danovaro et al.,
1999; Gili et al., 2000; Cartes et al., 2002). Detrital
27
material originating in the water column and on
the continental shelf flows along the channels
system in the Porcupine Seabight (Rice et al.,
1991), and organic matter sinks along with
inorganic particulate matter. Amounts of organic
matter may be higher in the channel systems than
surrounding areas affecting the distribution of
species and assemblages in the Seabight (Figs. 3
and 7; Cartes et al., 2002). Furthermore, pulses of
food arriving sporadically may tend to accumulate
in this channels system that acts as trap for
sediments (see Gili et al., 2000). Thus, these
fluctuations in food supply can generate a high
variability in patterns of abundance and distribution of species over time (see temporal variability
in Section 4.1).
4.3. Diversity
Diversity trends in the deep sea are very
variable. Various faunal groups have shown
different depth–diversity trends (e.g. Sanders and
Hessler, 1969; Rex, 1973, 1981; Carney and Carey,
1982; Cartes and Sardà, 1992; Paterson and
Lambshead, 1995; Allen and Sanders, 1996; Rex
et al., 1997; Howell et al., 2002). However, this
large variation might in part be a result of the
different collecting techniques and analytical
methods used for estimating diversity (Rex et al.,
1997). High diversity in the deep sea has been
attributed to environmental /or biological factors
(see for review Stuart et al., 2003).
A number of studies have found that gastropods
and protobranchs show parabolic trends in diversity, with peaks at upper rise depths
(2000–3000 m) (Rex, 1981, 1983; Rex et al.,
1997). However, Allen and Sanders (1996) reported different trends in the diversity of protobranchs from Atlantic basins, with diversity peaks
in deeper waters (3000–4000 m) followed by a
drop to the deepest parts of the basins (5000 m).
Also, in most basins there was a dip in diversity
between 2000 and 2600 m. In the Western
European basin, for example, diversity values
were high with a diversity minimum at about
2500 m and a maximum at 4400 m.
In this study, diversity did follow a concave
unimodal trend (Fig. 10) similar to trends
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C. Olabarria / Deep-Sea Research I 52 (2005) 15–31
previously shown for gastropods and bivalves
(Rex, 1981, 1983; Rex et al., 1997). This diversity
pattern is similar to that found for seastars in the
Porcupine Seabight (Howell et al., 2002), although
diversity of this group reached maximum values at
1800 and 4700 m. Furthermore, the observed
pattern matched that exhibited by protobranchs
from some Atlantic basins (Allen and Sanders,
1996). Nevertheless, diversity values were not as
high as those found in the West European Basin
by the latter authors.
The low values of diversity between 2100 and
2700 m were due in part to the large numbers of
individuals of Kelliella atlantica in some of the
samples collected at these depths. For example,
this species accounted for 93% of individuals
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
per sample). Between 4800 and 4900 m, diversity
values dropped since the number of species
per sample was lower (4–9 species per sample).
These results indicate high values of diversity
at abyssal depths. Rex et al. (2005) proposed
the ‘‘source-sink hypothesis for abyssal biodiversity’’ suggesting that abyssal populations might
be maintained by immigration from adjacent
bathyal populations of species with high dispersal
ability. If so, this hypothesis, together with the
low impact of predation on bivalve species at
these depths (Allen and Sanders, 1996), could
explain in part the high diversity values found
at 4100 m. Furthermore, several studies reported
strong fluxes of organic matter to the Porcupine
Abyssal Plain (e.g. Thurston et al., 1998; Billett
et al., 2001; Fabiano et al., 2001). Although
seasonally variable, this supply of organic
matter at abyssal depths might be responsible
for the increase of diversity observed at 4100 m.
For instance, some trophic groups such as depositand suspension-feeders would be favoured by
this food supply. In fact, Thurston et al.
(1998) and Billett et al. (2001) found that
particle fluxes arriving at the sea floor on the
Porcupine Abyssal Plain were very important
in determining changes in the specific composition and abundance of megafaunal assemblages.
Acknowledgements
I would like to thank the officers and crews of
RSS Challenger and RSS Discovery, as well as the
colleagues who have been instrumental in collecting the samples used in this study. This research
has been supported by a Marie Curie Fellowship
of the European Community programme ‘‘Energy,
Environment and Sustainable Development’’ under contract EVK2-CT-2001-50010 to Celia Olabarria. In addition, I would also like to thank Dr
M Rex, Dr B Bett and Dr D Billett for their
valuable comments on the first draft of this
manuscript. I also thank the three anonymous
referees whose comments improved considerably
the original manuscript.
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