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BioMed Central
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BMC Ecology
Open Access
Research article
Biodiversity of nematode assemblages from the region of the
Clarion-Clipperton Fracture Zone, an area of commercial mining
interest
P John D Lambshead*
1
, Caroline J Brown
1,2
, Timothy J Ferrero
1
,
Lawrence E Hawkins
2
, Craig R Smith
3
and Nicola J Mitchell
1
Address:
1
Department of Zoology, The Natural History Museum, Cromwell Road, London, SW7 5BD, UK,
2
Department of Oceanography,
Southampton Oceanography Centre, Waterfront Campus, European Way, Southampton, SO14 3ZH, UK and
3
Department of Oceanography,
University of Hawaii at Manoa, 1000 Pope Road, Honolulu, HI96822, USA
Email: P John D Lambshead* - pjdl@nhm.ac.uk; Caroline J Brown - c1brown@uk.ibm.com; Timothy J Ferrero - tjf@nhm.ac.uk;
Lawrence E Hawkins - lawrence.e.hawkins@soc.soton.ac.uk; Craig R Smith - csmith@soest.hawaii.edu;
Nicola J Mitchell - n.mitchell@nhm.ac.uk
* Corresponding author
Abstract
Background: The possibility for commercial mining of deep-sea manganese nodules is currently
under exploration in the abyssal Clarion-Clipperton Fracture Zone. Nematodes have potential for
biomonitoring of the impact of commercial activity but the natural biodiversity is unknown. We
investigate the feasibility of nematodes as biomonitoring organisms and give information about their
natural biodiversity.
Results: The taxonomic composition (at family to genus level) of the nematode fauna in the abyssal
Pacific is similar, but not identical to, the North Atlantic. Given the immature state of marine
nematode taxonomy, it is not possible to comment on the commonality or otherwise of species
between oceans. The between basin differences do not appear to be directly linked to current
ecological factors. The abyssal Pacific region (including the Fracture Zone) could be divided into
two biodiversity subregions that conform to variations in the linked factors of flux to the benthos
and of sedimentary characteristics. Richer biodiversity is associated with areas of known
phytodetritus input and higher organic-carbon flux. Despite high reported sample diversity,
estimated regional diversity is less than 400 species.
Conclusion: The estimated regional diversity of the CCFZ is a tractable figure for biomonitoring
of commercial activities in this region using marine nematodes, despite the immature taxonomy (i.e.
most marine species have not been described) of the group. However, nematode ecology is in dire
need of further study.
Background
The area where there is the most interest in commercial
deep-sea mining lies within the Clarion-Clipperton Frac-
ture Zone (CCFZ) in the abyssal Pacific west of Central
America. Three zones, in particular, are of especial com-
mercial importance, 8° 27'N, 150° 47' W; 11° 42' N,
138° 24' W; and 15° 00' N, 126° 00' W) Fig. 1. The Inter-
national Sea Authority is required to develop regulations
for mining to take place, including regulations for envi-
Published: 9 January 2003
BMC Ecology 2003, 3:1
Received: 19 September 2002
Accepted: 9 January 2003
This article is available from: http://www.biomedcentral.com/1472-6785/3/1
© 2003 Lambshead et al; licensee BioMed Central Ltd. This is an Open Access article: verbatim copying and redistribution of this article are permitted in
all media for any purpose, provided this notice is preserved along with the article's original URL.
BMC Ecology 2003, 3 http://www.biomedcentral.com/1472-6785/3/1
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ronmental monitoring. Such monitoring will involve sur-
veys of the benthic fauna.
The most abundant metazoan group in deep-sea sedi-
ments is the marine Nematoda [1]. Deep-sea nematode
assemblages are also highly diverse and species rich at lo-
cal (point diversity and alpha diversity sensu Gray [2])
scales [3] but estimates of regional and global species rich-
ness remain speculative [4,5]. The utility of nematodes as
monitoring organisms has been demonstrated in shallow
water studies where they are now used routinely in this
role [6,7].
There are, however, difficulties in utilising deep-sea nem-
atodes as monitoring organisms. The taxonomy of the
group is immature; few species have been described and
geographic coverage is uneven [5]. There are few nema-
tode taxonomic studies of the deep Pacific. An as yet un-
published taxonomic study of Pacific abyssal nematodes
of the Peru-Beckens region has been undertaken as part of
the DISCOL project [8]. 358 nematode specimens taken
from the ECHO I site within the CCFZ have been taxo-
nomically studied and 148 putative species discovered
[9]. It should be noted that although most deep-sea nem-
atode species have never been described, they can never-
theless be sorted into 'morphotypes' (morphological
operational taxonomic units) which are often considered
to be equivalent to species for the purpose of biodiversity
studies.
The study of deep-sea nematode biodiversity is in an early
stage. There have been no published biodiversity studies
at the species level on Pacific abyssal nematode fauna, and
only one on Pacific bathyal fauna [10]. Most studies have
Figure 1
Cluster analysis of samples on fourth root transformed data using the Bray-Curtis index of similarity and single linkage cluster-
ing. The samples are labelled according to the station from which they were collected.
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taken place in the North Atlantic and it is not clear how
similar nematode assemblages in the Atlantic are to those
in the mining regions in the Indo-Pacific [11]. Further-
more, studies have usually been made at individual sta-
tions rather than over larger areas, so regional diversity is
unknown but is assumed to be high because local diversi-
ty is high [4,5].
Deep-sea mining is likely to cause physical disturbance
and smothering [12]. Natural physical and smothering
disturbance, such as that resulting from turbidites and
benthic storms, has been associated with a small but sta-
tistically significant reduction in North Atlantic deep-sea
nematode diversity [13]. However, it was noteworthy that
the effect of disturbance could be prolonged (e.g., lasting
for decades to centuries), possibly through changes in sed-
iment composition. The robustness of deep-sea nematode
biodiversity to physical disturbance mirrors the conclu-
sions of studies on dredging impacts in shallow water
[14]. Such properties offer support for nematodes as mon-
itoring organisms in that nematode assemblages are
present for analysis at all levels of impact but display de-
tectable changes in composition. These properties, cou-
pled with high abundance and high sample/local diversity
are ideal characteristics of a monitoring taxon but if re-
gional diversity is high, then this, coupled with immature
taxonomy, could present significant difficulties for rou-
tine monitoring. This is the first data set that covers a suf-
ficient area to allow a credible estimation of regional
nematode species richness in the abyss, or indeed any-
where apart from the north-west coast of Europe.
This paper has two objectives. The first is to augment pre-
vious papers on nematode abundance, biomass and spe-
cies richness gradients [15,16] by making a preliminary
investigation of the nematode biodiversity from the re-
gion of the CCFZ. In addition, the taxonomic composi-
tion of the region will be compared to abyssal sites
previously investigated from the North Atlantic in order to
evaluate between basin patterns in nematode biodiversity.
The second objective of the study is to estimate deep-sea
nematode regional diversity for the first time so as to es-
tablish whether the total number of species likely to be en-
countered is tractable for routine biomonitoring of
commercial activities.
Results
In the central Pacific, twenty-five families were recorded
from the equatorial station and all were found at least at
one other station. The highest number of families was re-
corded from 2°N because of a family unique to that sta-
tion, the Tripyloididae. Subsequently, the number of
families decreased with increasing latitude to a minimum
of 21 families at 9 and 23°N. Dominant families (>10%
of total population in sample) recorded along the stations
were divided into two communities (Table 1). At stations
from 0–5°N, the dominant families were the Monhysteri-
dae, the Chromadoridae and the Microlaimidae. At sta-
tions from 9–23°N, the Monhysteridae and the
Chromadoridae were also dominant families, but the Xy-
alidae replaced the Microlaimidae. The Oxystominidae
were a subdominant family (>5%) at all stations and the
Microlaimidae were subdominant at stations at 9 and
23°N. At the 0–5°N stations, other subdominant families
varied from station to station (Table 1).
At the genus level, Thalassomonhystera dominated at all Pa-
cific stations, varying in abundance from 18% at the equa-
torial station, to 33% at 9 and 23°N (Table 2).
Acantholaimus also occurred with a high frequency at all
stations. Other dominant to subdominant genera (>5%
and >1% respectively) included Halalaimus, Microlaimus,
Molgolaimus, Leptolaimus and Aponema. The patterns of
dominant and subdominant genera varied from station to
station, but followed the general replacement of the Mi-
crolaimidae by the Xyalidae, between 5 and 9°N.
A total of 3,321 individuals were sorted into 200 species,
All but seven species could be assigned to known genera.
The domination of Thalassomonhystera was caused by
Table 1: Mean percentage of dominant (>10%) and subdominant (>5%) nematode families present in 0–1 cm sediment horizon from the
stations of the Clarion Clipperton Fracture Zone.
Equator 2°N 5°N 9°N 23°N
Monhysteridae 32% Monhysteridae 28% Monhysteridae 30% Monhysteridae 36% Monhysteridae 33%
Chromadoridae 10% Microlaimidae 21% Microlaimidae 24% Xyalidae 13% Xyalidae 18%
Microlaimidae 8% Chromadoridae 10% Chromadoridae 11% Chromadoridae 9% Chromadoridae 10%
Leptolaimidae 7% Xyalidae 7% Oxystominidae 5% Oxystominidae 6% Microlaimidae 9%
Xyalidae 6% Desmoscolecidae 6% Microlaimidae 6% Oxystominidae 6%
Aegialoalaimidae 6%
Meyliidae 5%
The families are listed in order of dominance per station.
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Table 2: Mean percentage of dominant (>5%) and subdominant (>1%) nematode genera present in the 0–1 cm sediment horizon from
the stations from the Clarion-Clipperton Fracture Zone.
Equator 2°N 5°N 9°N 23°N
Thalassomonhystera 18.3% Thalassomonhystera 22.9% Thalassomonhystera 22.8% Thalassomonhystera 32.5% Thalassomonhystera 32.1%
Acantholaimus 9.6% Microlaimus 7.1% Molgolaimus 8.5% Acantholaimus 5.9% Acantholaimus 7.3%
Quadricoma 5.7% Molgolaimus 6.8% Acantholaimus 7.6% Halalaimus 5.5% Linhystera 6.5%
Leptolaimus 5.5% Acantholaimus 5.7% Microlaimus 5.4% Microlaimus 4.1% Halalaimus 5.3%
Microlaimus 5.2% Desmoscolex 5.1% Aponema 4.6% Leptolaimus 4.1% Theristus 4.0%
Diplopeltoides 5.2% Aponema 4.8% Halalaimus 3.7% Linhystera 2.6% Aponema 3.5%
Halalaimus 3.5% Diplopeltoides 3.1% Quadricoma 2.8% Manganonema 2.6% Microlaimus 3.5%
Desmodora 3.2% Halalaimus 2.8% Desmodora 2.6% Diplopeltula 2.6% Leptolaimus 3.5%
Diplopeltula 3.0% Quadricoma 2.5% Leptolaimus 2.4% Aegialoalaimus 2.2% Aegialoalaimus 2.5%
Manganonema 2.7% Ascolaimus 2.3% Diplopeltoides 2.4% Quadricoma 2.2% Daptonema 2.3%
Thalassomonhystera 2.5% Syringolaimus 2.0% Ascolaimus 2.2% Prochromadorella 1.9% Manganonema 2.0%
Desmoscolex 2.2% Nox 2.0% Manganonema 2.0% Desmodora 1.9% Diplopeltoides 1.8%
Actinonema 2.0% Campylaimus 2.0% Syringolaimus 1.7% Diplopeltoides 1.9% Desmoscolex 1.8%
Camacolaimus 1.7% Actinonema 1.4% Tubolaimoides 1.7% Cobbia 1.9% Neochromadora 1.3%
Aponema 1.7% Desmodora 1.4% Cervonema 1.3% Syringolaimus 1.5% Pselionema 1.3%
Linhystera 1.2% Linhystera 1.4% Acantholaimus 1.1% Molgolaimus 1.5% Quadricoma 1.3%
Molgolaimus 1.0% Manganonema 1.4% Desmoscolex 1.1% Nox 1.1% Campylaimus 1.3%
Eudraconema 1.0% Rhips 1.1% Linhystera 1.1% Desmoscolex 1.1% Actinonema 1.0%
Campylaimus 1.0% Eudraconema 1.1% Amphimonhystera 1.1% Desmodora 1.0%
Pselionema 1.1% Molgolaimus 1.0%
Metadesmolaimus 1.0%
Southerniella 1.0%
The genera are listed in order of dominance at each station.
Table 3: Mean percentage of dominant (>1%) nematode species present in 0–1 cm sediment horizon at the stations from the Clarion
Clipperton Fracture Zone.
Equator 2°N 5°N 9°N 23°N
Thalassomonhystera sp.
.A
5.4% 5.3% 10.0% 7.3% 13.3%
Thalassomonhystera sp.
.B
6.0% 2.3% 3.8% 7.0% 5.0%
Thalassomonhystera sp.
G
0% 3.3% 1.3% 8.3% 9.5%
Acantholaimus sp. .A 2.6% 3.0% 2.8% 4.7% 2.8%
Molgolaimus sp. B 1.0% 4.8% 6.6% 2.0% 2.0%
Aponema sp. A 1.4% 4.25% 2.4% 0% 4.7%
Microlaimus sp. .B 1.8% 3.8% 1.0% 5.0% 3.5%
Thalassomonhystera sp.
D
2.5% 4.8% 2.8% 0% 0%
Diplopeltoides sp B 3.0% 2.5% 2.7% 0.7% 1.7%
Acantholaimus sp. B 2.6% 0% 3.8% 0% 0%
Microlaimus sp. A 4.0% 5.0% 2.0% 0% 0%
Linhystera sp. A 1.25% 0% 1.0% 3.5% 6.5%
Quadricoma sp. A 2.3% 2.3% 2.5% 2.5% 1.0%
Quadricoma sp. C 2.4% 0% 1.5% 1.0% 2.0%
Halalaimus sp. D 1.2% 2.0% 4.0% 1.5% 2.0%
Desmoscolex sp. .A 1.0% 2.8% 1.7% 1.0% 2.0%
Manganonema sp. A 2.8% 2.5% 1.8% 1.0% 2.0%
Leptolaimus sp. B 3.7% 1.0% 2.5% 1.5% 3.3%
Acantholaimus sp. C 1.0% 2.3% 0% 0% 4.3%
The species are listed in order of dominance from the whole data set.
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more than one species (Table 3). Three species of this ge-
nus were dominant across the stations (with one excep-
tion) and an additional species was dominant in the
phytodetritus-influenced stations at 0°N, 2°N, and 5°N.
Many genera were represented by more than one species
(Table 4). Five genera included 22% of the species, and
ten genera contained 33% of the species.
Similar dendrograms were obtained from both the un-
transformed and transformed data. This is not unexpected
because the samples showed a high equitability and the
percentage dominance of the most abundant species was
low. Therefore, only the dendrogram for the transformed
data is depicted here to save space, transformed data being
commonly employed in this type of analysis (Fig. 1).
The first split in the dendrogram at approximately 40% di-
vided the samples into two regions, the southern phytode-
tritus-influenced region from 0°N to 5°N and the
northerly region from 9°N to 23°N. The northerly two
stations did not separate, although the 23°N HOT station
formed a cluster at the 55% level. The southern samples
split into the three stations, with one exception, but did
not cluster according to geography. Instead, the 0°N sta-
tion was most similar to the 5°N station. The topography
of the dendrogram was 'flat', with samples being only
slightly more similar to each other than either station or
region splits, indicating high variability between the sam-
ples.
Neither the species accumulation per number of individ-
ual curves for the whole region nor either of the two sub-
regions came to asymptote indicating that the sampling
had been insufficient to discover regional diversity (Fig.
2). The curves do indicate beta diversity, the differentia-
tion diversity, between samples (i.e. the rate of change of
species between samples), across the CCFZ and the two
subregions. The northern non-phytodetritus subregion is
noticeably less beta-diverse.
A sigmoidal growth model best fitted the species accumu-
lation curves for the whole data set and the southern sub-
region, stations 0°N, 2°N, & 5°N. A Hoerl model best
fitted the northern subregion data (r = 0.99998) but the
sigmoidal model was almost as good a fit so was also used
for estimating species richness in this subregion also for
consistency. The estimated maximum number of species
for each data set is shown in Table 5.
The results for non-parametric statistical estimators are
shown in Table 6. They tend to give slightly lower esti-
mates for species richness than the sigmoidal growth
model suggesting that the curve extrapolation is not un-
derestimating regional species richness across the transect.
Table 4: Genera with three or more species (in brackets) recorded from various locations; (i) Clarion-Clipperton Fracture Zone (CCFZ,
this study), (ii) Porcupine Abyssal Plain 1989 study (PAP) [45], (iii) San Diego Trough (SDT) [10], (iv) Rockall Trough 535 metre station
(RT 535) [10], (v) Irish Sea (IS, Ferrero unpublished data) [3], and (vi) Clyde Inland Sea low water spring tide (CIS) [6].
CCFZ PAP 1989 SDT RT535 IS CIS
Thalassomonhystera 12 Acantholaimus 8 Daptonema 8 Thalassomonhystera 7 Daptonema 8 Daptonema 8
Halalaimus, 11 Halalaimus 8 Halalaimus 7 Halalaimus 5 Microlaimus 7 Theristus 8
Acantholaimus 7 Daptonema 4 Microlaimus 6 Daptonema 3 Halalaimus 5 Microlaimus 5
Desmodora 7 Diplopeltula 4 Ceramonema 4 Microlaimus 3 Sabatieria 5 Neochromadora 4
Leptolaimus 7 Thalassomonhystera 4 Desmodora 4 Metadesmolaimus 3 Paracanthonchus 4 Cyartonema 3
Diplopeltoides 5 Microlaimus 3 Leptolaimus 3 Tricoma 3 Pomponema 4 Dichromadora 3
Syringolaimus 5 Oxystomina 3 Molgolaimus 3 Prochromadorella 4 Metadesmolaimus 3
Cervonema 4 Quadricoma 3 Prochromadorella 3 Theristus 4 Pomponema 3
Desmoscolex 4 Ceramonema 3
Diplopeltula 4 Desmodora 3
Linhystera 4 Richtersia 3
Oxystomina 4 Tricoma 3
Ascolaimus 3
Campylaimus 3
Campylaimus 3
Cobbia 3
Litinium 3
Marylynnia 3
Microlaimus 3
Molgolaimus 3
Note that the Rockall data are based on only 3 samples so may underestimate numbers of species per genus. All other data are based on at least six
samples.
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Discussion
The presence of a number of closely related and apparent-
ly morphologically similar species in the same local area
has been noted as a characteristic of marine nematode
fauna in shallow water studies [17]. However, this phe-
nomenon is particularly exaggerated in the CCFZ (Table
4).
At the family level, there was a high degree of similarity in
nematode community composition in these samples with
only a small variation between the southern three phyto-
detritus-influenced and the northern two non-phytodetri-
tus influenced regions. The non-phytodetritus influenced
northern areas showed an increase in the percentage of
Xyalidae compared to the southern three stations.
The dominant families recorded here are broadly similar
to those from other abyssal data. Where there are differ-
ences, they seem to be associated more with biogeography
than with the environment, see Table 7. For example, in
the Pacific Monhysteridae dominate the stations, irrespec-
tive of the apparent influence of phytodetritus. In the
North Atlantic, Chromadoridae dominate despite each
station being influenced differently by a number of factors
including phytodetritus flux [11], turbidites and benthic
storms [13] all of which have been shown to be associated
with variation in deep-sea nematode diversity.
Figure 2
Plots of the species accumulation curves against numbers of individuals for the whole data set (diamonds), the southern phyto-
detritus-influenced samples (squares) and the northern samples (triangles).
0
50
100
150
200
250
0 500 1000 1500 2000
Numbers of individuals
Species richness
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The association with biogeography rather than with local
ecological factors implies that the differences in the pro-
portions of the communities taken up by the dominant
families are the product of historical processes rather than
of current ecology. This is unexpected because the domi-
nant families from each ocean basin are usually consid-
ered to be in different trophic groups. Deep-sea
Monhysteridae tend to be small mouthed organisms, such
as Thalassomonhystera, that presumably feed on bacteria or
other small particles. In contrast, deep-sea Chromadori-
dae, such as Acantholaimus or Prochromadorella, tend to
have buccal armature that is capable of piercing or scrap-
ing. The feeding preference of deep-sea members of this
family is unknown but at least some of their shallow water
relatives are associated with diatom feeding, the teeth be-
ing used to pierce or break the frustrule [18–23]. It is
worth emphasising that observations on marine nema-
tode feeding have been limited to a handful of opportun-
istic coastal species that can be cultured, so their feeding
ecology may not be typical of offshore family members.
Also, deep-sea Chromadoridae are dominated by the ge-
nus Acantholaimus (see below), which is rare in shallow
water, while shallow-water Chromadoridae are typically
dominated by Dichromadora and Neochromadora which are
less common in the deep sea. Nevertheless, this apparent
trophic variation between the ocean basins suggests that
either there are errors in our comprehension of nematode
trophic groups or that there have been powerful historical
forces affecting the distribution of these groups that has
left an imprint that is still detectable.
Table 5: Estimations of regional species richness using an extrapolation of an MMF model (y = (ab + cx
d
)/(b + x
d
) of a plot of species
accumulation per number of individuals at near asymptote at 10
8
individuals. The r is a measure of the 'fit' of the model to the data.
Data Sigmoidal Growth Model Parameters r Estimated Species Richness
All Samples a = -12.1378 b = 154.4177 c = 360.9705 d = 0.7323 0.99999 361
Southern Samples (O°N, 2°N & 5°N) a = -16.7132 b = 109.1754 c = 385.8644 d = 0.6642 0.99997 386
Northern Samples (9°N & 23°N) a = 12.6610 b = 485.3579 c = 158.5034 d = 1.0503 0.99996 159
Table 6: Non-parametric statistical estimators of species richness from Colwell's EstimateS program [47].
Data ICE Chao 2 Jackknife 2
All Samples 281 280 313
Southern Samples (O°N, 2°N &
5°N)
264 260 287
Northern Samples (9°N & 23°N) 139 129 147
Table 7: Dominant nematode families present in a number of abyssal stations. CCFZ = Clarion-Clipperton Fracture Zone (this study),
PAP = Porcupine Abyssal Plain [28], MAP = Madeira Abyssal Plain [28], HEBBLE = Scotian Rise [48], HAP = Hatteras Abyssal Plain
[27].
Station Dominant Family Subdominant Families Ecological Notes Geographic Location
CCFZ 0°N Monhysteridae Chromadoridae Microlaimidae Phytodetritus influenced Central Pacific
CCFZ 2°N Monhysteridae Microlaimidae Chromadoridae Phytodetritus influenced Central Pacific
CCFZ 5°N Monhysteridae Microlaimidae Chromadoridae Phytodetritus influenced Central Pacific
CCFZ 9°N Monhysteridae Xyalidae Chromadoridae Central Pacific
CCFZ 23°N Monhysteridae Xyalidae Chromadoridae Central Pacific
HEBBLE Chromadoridae Xyalidae Oxystominidae Benthic Storms Northwest North Atlantic
PAP 1989 Chromadoridae Xyalidae Monhysteridae Phytodetritus influenced Northeast North Atlantic
PAP 1991 Chromadoridae Monhysteridae Xyalidae Phytodetritus influenced Northeast North Atlantic
MAP Chromadoridae Xyalidae Monhysteridae Turbidite Northeast North Atlantic
HAP Chromadoridae Xyalidae Oxystominidae Southwest North Atlantic
Ecological factors that might influence nematode communities are listed, where they are known.
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The genera discovered at the CCFZ were mostly familiar to
science and the common genera have also been found
commonly in North Atlantic abyssal fauna, notably Tha-
lassomonhystera, Halalaimus, and Acantholaimus (Table 8)
and we may conjecture that these genera are characteristic
of abyssal nematode communities, although Thalassomon-
hystera is more important in the Pacific data and Acan-
tholaimus in the Atlantic. Although phytodetritus and
physical disturbance have been shown to influence nem-
atode species richness [11,13,15], there is little evidence
of characteristic dominant genera associated with the
presence or absence of these factors.
There was no evidence that the type of core sampler used
had influenced the analysis, clusters did not group accord-
ing to core sampler employed. The low similarity between
samples from the same station demonstrates a high de-
gree of variability between samples. The stations split
weakly into two regions, divided between the southern
three stations and the northern two. This was not a simple
question of geographical distance as the distance is greater
between 9°N and 23°N than between 5°N to 9°N, where
the putative ecotone occurred. This division is associated
both with the presence or absence of phytodetritus and
the concomitant change in sediment structure. Both fac-
tors have been previously associated with deep-sea nema-
tode species distributions [24–29].
It is noteworthy that the high 'point' (i.e. sample) diversity
recorded for deep-sea systems is not reflected in the re-
gional species-richness estimates. The estimated regional
species diversity in the CCFZ is not especially high and is
tractable for biodiversity analysis both for monitoring and
scientific research. The CCFZ is an open system so the rar-
er species in the assemblage are likely to be somewhat dif-
ferent with each programme of work, changing with space
and time. It should also be pointed out that this estimate
is based on identifications using only light microscopy
and does not incorporate the additional taxonomic reso-
lution that might be determined using ultrastructure or
molecular analysis. It is quite conceivable that sibling spe-
cies remain undetected by light microscopy identification
[30].
A higher estimated species richness was found in the
southern phytodetritus-influenced stations than in the
northern stations, reflecting the point (sample) species
richness and diversity analysis [16]. However the fit of the
model to the northern data was less good so there may be
increased error in the calculation for this region. It is sus-
picious that a Hoerl model (which lacks a maxima) best
fitted this data suggesting that the region may have been
woefully under-sampled for estimating regional diversity.
Conclusions
The higher taxa in the region of the CCFZ are typical of the
better known North Atlantic abyss but the relative abun-
Table 8: Mean percentage of dominant (>5%) and subdominant (>1%) nematode genera present in 0–1 cm sediment horizon from the
stations from the northeast North Atlantic [28].
PAP 1989 PAP 1991 MAP
Acantholaimus 15.2% Thalassomonhystera 17.3% Acantholaimus 24.0%
Thalassomonhystera 15.0% Acantholaimus 12.0% Thalassomonhystera 11.7%
Halalaimus 9.0% Halalaimus 7.0% Daptonema 11.5
Elzalia 6.4% Prochromadorella 6.4% Halalaimus 11.1
Chromadorina 5.0% Enchonema 6.3% Metadesmolaimus 3.5
Quadricoma 4.7% Daptonema 5.2% Campylaimus 3.5
Daptonema 4.4% Pareudesmoscolex 4.3% Amphimonhystrella 3.0
Campylaimus 4.1% Desmoscolex 3.9% Pomponema 1.6
Microlaimus 3.9% Molgolaimus 3.8% Quadricoma 1.6
Desmoscolex 2.7% Campylaimus 3.8% Chromadora 1.4
Actinonema 2.0% Quadricoma 3.0% Cyartonema 1.4
Aegialoalaimus 1.9% Elzalia 2.6% Desmoscolex 1.4
Prochromadora 1.8% Diplopeltua/ Diplopeltoides 2.6% Actinonema 1.2
Linhystera 1.6% Diplolaimella/ Diplolaimelloides 1.7% Innocuonema 1.2
Metadesmolaimus 1.5% Pareudesmoscolex 1.6% Dolichoalaimus 1.1
Diplopeltula 1.4% Manganonema 1.6% Syringolaimus 1.1
Scaptrella 1.3% Karkinochromadora 1.3% Diplopeltoides 1.1
Pierrickia 1.3% Aegialoalaimus 1.1%
Amphimonhystrella 1.0% Amphimonhystrella 1.1%
The genera are listed in order of dominance per station. PAP = Porcupine Abyssal plain, MAP = Madeira Abyssal Plain.
BMC Ecology 2003, 3 http://www.biomedcentral.com/1472-6785/3/1
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dance of any particular family or genus is different be-
tween the oceans, possibly because of historical rather
than ecological processes. So extant nematode biodiversi-
ty data from North Atlantic abyssal depths may not be en-
tirely representative of baseline conditions in the Pacific
even where the local environmental factors are similar.
The region spanning from the equator to 23°N can be fur-
ther sub-divided into subregions based on nematode bio-
diversity differences that are associated with differences in
the sediment and in the organic flux. The low estimated
regional diversity is a tractable figure for the biomonitor-
ing of commercial activities in this region using marine
nematodes despite the immature taxonomy of the group.
However, a lack of natural history data will limit the eco-
logical inferences that could be drawn from changes to
nematode community structure.
Methods
The study area is shown in Fig. 3. Sediment samples were
collected at four "EqPac" sites along a latitudinal gradient
of phytodetrital deposition and organic-carbon flux from
0 to 9°N at 140°W in the central equatorial Pacific, as part
of the US Joint Global Ocean Flux Study (JGOFS). A visi-
ble input of phytodetritus has been reported at the sta-
tions at 0, 2 and 5°N on the 140°W transect [31]. The
presence of measurable quantities of chlorophyll a and
excess
234
Thorium (tracers with degradation time-scales
of less than one hundred days, phytoplankton with intact
chloroplasts, and high respiration rates of associated mi-
crobial populations, implied that this material was recent-
ly settled and undegraded [31–33]. In contrast, at 9°N,
the surface detritus appeared to be much more refractory
in nature. Overall, the annual abyssal, particulate organic
carbon (POC) flux exhibits a four-fold increase between
9°N and the equator [34,35] giving 'large latitudinal gra-
dients in biogenic particle flux to the abyssal seafloor'
[36].
A site at 23°N, 158°W, beneath the Hawaii Ocean Time
Series (HOT) site, was also considered a non-phytodetri-
tus site, as only a thin veneer of phytodetrital material was
recorded from the seafloor at this site and on only one oc-
casion. The deep carbon flux at 23°N was similar to the
9°N site [37].
All five stations were located on predominately flat, sedi-
ment-covered abyssal plain. Earlier studies indicated that
they were positioned along a gradient of overlying prima-
ry productivity, POC flux and sediment accumulation rate
[38]. As far as is known, all other environmental variables
were approximately constant. Sampling locations, collec-
tion dates and water depths are listed in Table 9, Fig.
3[15]. The maximum distance between the stations is
3,195 km, or 2,523 km of latitude, which should be ade-
quate to estimate regional diversity.
At the southern stations, 0°N, 2°N and 5°N, the sediment
consisted of predominantly calcareous foraminiferal
Table 9: Sample locations, water depths, collecting date and device.
Sample Location Water Depth (m) Collecting Date Collecting Device
BC4 00°06.00'N 139°43.90'W 4328 15/Nov/92 Box Corer
BC6 00°06.62'N 139°43.96'W 4305 16/Nov/92 Box Corer
BC7 00°06.40'N 139°44.10'W 4307 18/Nov/92 Box Corer
BC8 00°06.98'N 139°43.94'W 4301 19/Nov/92 Box Corer
MC15 00°06.57'N 139°43.42'W 4304 19/Nov/92 Multiple Corer
BC9 02°03.94'N 140°08.94'W 4409 20/Nov/92 Box Corer
BC10 02°04.00'N 140°07.90'W 4414 21/Nov/92 Box Corer
BC11 02°03.96'N 140°08.06'W 4409 22/Nov/92 Box Corer
BC12 02°03.80'N 140°07.90'W 4410 23/Nov/92 Box Corer
BC15 05°05.00'N 139°39.00'W 4447 27/Nov/92 Box Corer
BC16 05°04.42'N 139°38.90'W 4446 28/Nov/92 Box Corer
BC17 05°04.80'N 139°38.50'W 4424 29/Nov/92 Box Corer
BC18 05°04.20'N 139°38.40'W 4320 30/Nov/92 Box Corer
MC26 05°04.30'N 139°38.30'W 4418 30/Nov/92 Multiple Corer
BC19 08°55.08'N 139°52.20'W 4986 3/Dec/92 Box Corer
BC20 08°56.04'N 139°51.55'W 4994 4/Dec/92 Box Corer
BC22 08°55.80'N 139°52.30'W 4991 6/Dec/92 Box Corer
MC1 22°54.69'N 157°49.74'W 4880 29/Jul/92 Multiple Corer
MC2 22°54.95'N 157°49.93'W 4871 29/Jul/92 Multiple Corer
MC4 22°54.74'N 157°50.21'W 4880 31/Jul/92 Multiple Corer
MC6 22°54.64'N 157°49.86'W 4884 1/8/92 Multiple Corer
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Page 10 of 12
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muds At the two northern stations, 9°N and 23°N, the
sediment consisted of fine-grained clays which more uni-
form in size [32,38]. Manganese nodules were present
only at the 9°N station. The sediment at the three south-
ern stations had
234
Thorium bioturbation rates that were
greater than at 9°N (mean D
b
values of 9.07 and <0.63)
indicating a greater rate of sediment mixing [32].
Previous work has suggested that the stations could be an-
alysed either as a transect of declining productivity or as
two regions, a southern region that experienced noticea-
ble phytodetritus input and a northern region that did not
[13].
Samples were obtained using either a multiple-corer with
10-cm diameter tubes or a USNEL-type box-corer divided
in situ into 10 × 10 cm subcores [39–41]. Box-cores can be
inefficient collectors of meiofauna [42]. Analysis of these
samples in earlier studies did not suggest sampler bias due
to the two collecting methods was a problem for abun-
dance[15] or species richness [16].
Following sampler recovery, cores were sliced at one cen-
timetre vertical intervals and transferred to buffered for-
maldehyde, diluted to 4% v/v with seawater. A single
multiple-core tube or box-core subcore was used per de-
ployment. Overlying top water was combined with the 0–
1 cm sediment layer. Nematodes were extracted using a
modified Ludox-TM
§
flotation method on a 45 µm sieve.
All nematodes extracted from the sediments were mount-
ed in anhydrous glycerine and are deposited in The Natu-
ral History Museum, London. Approximately 100
individuals were selected at random from the 0–1 cm sed-
iment horizon for identification from each sample as
Figure 3
The Clipperton Clarion Fracture Zone in the central eastern Pacific showing the area where there is interest in deep-sea min-
ing. The small squares show the stations from which samples were taken for this study.
BMC Ecology 2001, 3 http://www.biomedcentral.com/1472-6785/3/1
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there were too many nematodes recovered to identify
them all [15]. This approach should help offset possible
bias caused by inefficient collection in box cores, assum-
ing such bias to be random with respect to species identi-
ty. Individuals were identified to genus level and sorted
into morphotypes, which were considered to be identical
to species, using the pictorial key to world genera devel-
oped by Platt and Warwick and also the wider taxonomic
literature [43].
The nematode community composition was compared at
the species level, using cluster analysis based upon the
Bray-Curtis index of similarity and single linkage [44].
This is a hierarchical agglomerative clustering method
[45]. The analysis was repeated after fourth root transfor-
mation of the data, reducing the influence of the domi-
nant species. The BDPro program was used for cluster
analysis [46].
Regional species richness was estimated by species per
sample accumulation curves plotted against abundance,
with order of sample input randomised 50 times to re-
move distortions due to the stations lying along a produc-
tivity gradient; productivity is known to affect deep-sea
nematode diversity [5,16]. Colwell's EstimateS program
was employed for this purpose.
Models were fitted to the resulting curves using non-linear
regression in the shareware CurveExpert program, Table 5.
The sigmoidal growth model (y = (ab + cx
d
)/(b + x
d
), gave
the best fit to the total data and the southern region. The
Hoerl model best fitted the northern region, this is a con-
vex (or concave) power model that lacks inflection points
or maxima (or minima).
There are a variety of non-parametric statistical approach-
es for estimating species richness from incomplete sam-
pling using presence absence data [47]. These have been
tested and reviewed for forest biodiversity. Estimator accu-
racy is reduced by patchy spatial distributions and deep-
sea marine nematode data is known to be patchy [28,29]
so the results of this analysis must be treated with caution.
Some estimators are more robust than other to patchiness,
notably ICE and Chao2. ICE, Chao2 and Jackknife 2 are
also relatively insensitive to sample size [47] so these
three estimators were deemed most suitable for this data.
Second order Jacknife and Chao 2 estimators are based on
the numbers of duplicates and singletons and the number
of samples. ICE is an incidence-based coverage estimator
where the sample coverage estimate is the proportion of
all individuals in infrequent species that are not uniques.
Chao2 and ICE tend to overestimate when patchiness is
high whereas Jackknife 2 tends to be more stable for
patchy than random distributions where it tends to over-
estimate. In general ICE gives the best estimate but it is
useful to check the result against the other two estimators
[47]. Colwell's EstimateS program was used for the calcu-
lations.
Authors' contributions
This paper was produced from the PhD thesis of CJB, su-
pervised by LEH. PJDL conceived and supervised the
project, carried out the species richness part of the analysis
and wrote the paper. TJF supervised the taxonomy and
NJM the laboratory analysis. CRS helped conceive and su-
pervise the project, and conducted the field sampling.
Acknowledgements
The authors are grateful to Adam Cook for his advice and help in carrying
out this study and for reading the manuscript. The work was funded in part
by a Fulbright Commission scholarship and by US NSF grant no. OCE 90-
22116 to CRS. The authors acknowledge the assistance of the International
Seabed Authority for providing a venue and framework for discussion. This
is contribution no. 6078 form SOEST, and no. 848 from the US JGOFS pro-
gram.
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