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Continental Shelf Research 29 (2009) 2222–2233
Contents lists available at ScienceDirect
Continental Shelf Research
journal homepage: www.elsevier.com/locate/csr
Small-scale, patchy distributions of infauna in hydrodynamically mobile
continental shelf sands: Do ripple crests and troughs support
different communities?
Patricia A. Ramey , Judith P. Grassle, J. Frederick Grassle, Rosemarie F. Petrecca
Institute of Marine and Coastal Sciences, Rutgers, The State University of New Jersey, 71 Dudley Road, New Brunswick, New Jersey 08901, USA
a r t i c l e in f o
a b s t r a c t
Article history:
Received 17 March 2009
Received in revised form
21 August 2009
Accepted 27 August 2009
Available online 19 September 2009
Spatial variability of infauna with respect to distribution of topographic habitat features was examined
in hydrodynamically mobile sandy sediments on the inner continental shelf off New Jersey, USA (391
27.690 N, 741 15.810 W). Sediment cores for infauna were taken by SCUBA divers at multiple spatial scales
over time at 12-m depth in the LEO-15 research area on Beach Haven Ridge. Crests, troughs and less
consistently flanks of sand ripples 5–15-cm in height, were characterized by different infaunal
community patterns at spatial scales of centimeters to kilometers on several sampling dates. Overall,
infaunal community differences among ripple crests, troughs, and/or flanks within areas o 1-m2 were
greater than those found for each of these habitats (i.e., either crests, troughs, or flanks) that were
separated by distances of 2 m–4 km. Infaunal density and species richness were consistently higher in
troughs compared to crests. Indirect measures of food resources such as particulate organic carbon, chl
a, and pheophytin were associated with ripple crests and troughs. Troughs contained significantly
higher levels of particulate organic carbon ( 1.2 times higher) associated with finer sediments,
compared with crests and flanks. Various combinations of taxa had higher densities in either crests or
troughs of sand ripples depending on date, and the relative abundances of three taxa, the depositfeeding polychaete Polygordius jouinae, the suspension-feeding surfclam Spisula solidissima, and
predatory nemerteans were important in distinguishing between crests and troughs on most dates.
Thus, a priori knowledge of whether a benthic sample comes from a crest or trough helped to explain
small-scale infaunal patchiness in relatively homogeneous, subtidal sandy sediments. Consideration of
such topographic features in sampling designs can help in explaining variation in species’ distributions
at several spatial and temporal scales.
& 2009 Elsevier Ltd. All rights reserved.
Keywords:
Rippled beds
Topography
Habitat
Macrofauna
Polygordius
Spisula
1. Introduction
Infaunal organisms are intimately associated with the sediment in which they live. Therefore one would expect strong
relationships between sediment properties, and species distributions and abundances (reviewed by Snelgrove and Butman, 1994).
In the present study, community variability is examined in
relation to multiple topographic habitat features and sediment
properties at a variety of spatial scales over time.
Habitat characteristics influencing the structure and dynamics
of populations and communities have been emphasized for both
terrestrial and marine environments (e.g., Able et al., 2003; Diaz
et al., 2003; Morris, 2003; Zajac et al., 2003; Zajac, 2008).
Availability, quality, size, and spacing of habitat patches have
direct effects on populations or communities by providing
Corresponding author. Tel.: + 1732 932 6555x311; fax: + 1732 932 8578.
E-mail addresses: [email protected] (P.A. Ramey), jgrassle@marine.
rutgers.edu (J.P. Grassle), [email protected] (J.F. Grassle), petrecca@
marine.rutgers.edu (R.F. Petrecca).
0278-4343/$ - see front matter & 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.csr.2009.08.020
suitable living conditions (often species specific) in some areas
but not others (Chapman, 1994; Underwood et al., 2000). Indirect
effects include interactions among individuals or species (Menge
et al., 1985; Fairweather, 1988). It is well known that the scale of
sampling, relative to the distributional pattern of organisms, can
influence both the precision and interpretation of data (Thrush
et al., 1994). Studies of population and community patterns within
the context of defined habitats occurring at repeated intervals in
space, have been more common in terrestrial and intertidal
landscapes where species distributions and habitats are readily
visible (e.g., Kent et al., 1997; Underwood and Chapman, 1998).
Due to logistical constraints, research on subtidal macrofaunal
communities has more often focused on scale-dependent factors
without adequately defining or quantifying habitat(s) over time or
space (Zajac et al., 2003; Zajac, 2008) (but see Rogal et al., 1978).
Most commonly, spatial distributions and composition of
subtidal habitats and infaunal communities have been inferred
from point samples randomly collected via remote or ‘‘blind’’
bottom grabs with little explicit a priori consideration given to
habitat type other than sediment grain size distributions (Zajac
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et al., 2003). An outstanding feature of soft-sediment infaunal
communities is that both abundances and species composition
vary greatly at a variety of spatial scales (cm to km) (e.g.,
Volckaert, 1987; Morrisey et al., 1992), and patchy distributions
are very common at small scales (cm–m) even when sediment
grain size appears homogeneous (e.g., Sandulli and Pinckney,
1999). Such patchiness can confuse interpretation of community
pattern, especially if patterns are documented with samples
collected at scales larger than those relevant to the infauna. Hall
et al. (1994) observed that samples from subtidal, soft-sediments
are not generally taken with sufficient spatial resolution to
examine small-scale differences in community structure.
Advances in imaging techniques have shown that habitats in
subtidal, soft-sediment landscapes are heterogeneous and complex (e.g., Able et al., 2003; Diaz et al., 2003; Zajac et al., 2003;
Zajac, 2008). In shallow continental shelf environments, such as
the LEO-15 research site (Long-term Ecosystem Observatory at
15-m depth) on the inner shelf off New Jersey, waves, storms, and
stronger than average currents (average 5 cm s 1) create a sandy,
rippled bed with varying ripple wavelengths and heights and over
space and time (e.g., Traykovski et al., 1999; Styles, 1998; Able
et al., 2003). The morphology of ripples may be important in
explaining the spatial distribution of benthic microalgae and
infauna in sediments disturbed by waves (Kendrick et al., 1998),
and heterogeneity created by ripples may be a source of
microhabitat specialization and resource partitioning (Hogue
and Miller, 1981; Kendrick et al., 1998; Ramey and Bodnar, 2008).
One goal of the present study was to determine whether
community patterns at relatively small scales (i.e., cm–m) in
hydrodynamically mobile, sandy continental shelf sediments can
be associated with defined topographic features, and what
features of these habitats (e.g., sediment properties) are related
to observed infaunal patterns. Camera and video images from a
single inshore station at LEO-15 (Station 9) were used to define
and characterize habitats that were frequently encountered at
small scales of o1 m along a 44-m transect. Defined habitats
included ripple crests, flanks, troughs with bivalve shell hash in
them (+ SH), and troughs without shell hash (–SH). A suite of
sediment properties including grain size and indirect measures of
food availability (e.g., chl a, pheophytin, particulate organic
carbon, and nitrogen) were also quantified for each habitat
coincident with infaunal sampling to aid in understanding
observed patterns. To determine whether crest and trough
community patterns were detectable at larger spatial scales
(m–km) and whether observed patterns were consistent over
time (sampling dates), a previously collected, comparable infaunal
dataset was re-analyzed to specifically address community
patterns in rippled beds for the first time. Specific questions
asked were: (1) do infaunal communities inhabiting crests of
ripples differ from those in troughs (–SH and + SH) or flanks?; (2)
at what scale(s) ( o1 m–4 km) are community patterns (i.e.,
species composition and abundance) observed?; (3) what species
and sediment properties are most important in driving observed
differences in community structure?; (4) are community patterns
and the species responsible for them consistent over time and
space?
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Haven Ridge (391 280 N, 741 150 W), a shore oblique sand ridge
typical of the 71 such ridges found off the New Jersey coast
(McBride and Moslow, 1991). Research stations examined in the
present study included Station 9 located inshore on the southern
landward side of the ridge at 12-m depth (391 27.690 N, 741
15.810 W) and Station 30 located on the offshore flank of the Ridge
at 16-m depth (Station 30: 391 28.80 N, 741 13.290 W), 4 km
northeast of the inshore station (Fig. 1). Comparison of sediment
grain size between these two stations in 1990 indicated that they
were similar, with slightly coarser sediments offshore at Station
30 (mean grain size Station 9: 500 mm [F =1.0]; Station 30: F = 0.9)
(Craghan, 1995). Like other physically active shelf areas, rippled
beds are the predominant habitat feature (Twichell and Able,
1993; Able et al., 2003).
2.2. Sampling design
2.2.1. Small-scale (cm–m), single date June 2005
In July and August 2004, a SCUBA diver-operated, handheld
video camera was used to record the benthic environment at
Station 9 (Fig. 1). Habitats present within 1-m2 plots were defined
and characterized. On 9 June, 2005 a 44-m transect was set up at
Station 9 perpendicular to the ripples and prevailing current.
Along the transect a nested sampling design was used with a
series of successively smaller spatial scales nested within larger
scales (Fig. 2A). Spatial scales of interest included o1, 2, and 4 m.
Four infaunal core samples were taken from each of 12, 1-m2
quadrats on either the left or right side of the transect
(determined randomly by a coin toss), using a handheld corer
(7-cm diameter, 10-cm deep, 38.5 cm2) (Fig. 2A). Infaunal cores
were taken from four of five habitats present in 2004
(1 core habitat 1 =4 cores quadrat 1, n= 48). Habitats sampled
2. Materials and methods
2.1. Study site
This research was conducted on the inner continental shelf at
the Rutgers University Long-term Ecosystem Observatory at 15-m
depth (LEO-15), located 9 km off southern New Jersey (391
27.690 N, 741 15.810 W) (Fig. 1). This area is dominated by Beach
Fig. 1. Bathymetry of Beach Haven Ridge at LEO-15 showing sampling stations
Station 9 on inshore side of ridge and Station 30 offshore flank of the ridge
(modified from Twichell and Able (1993); same as in Weissberger and Grassle
(2003)).
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Fig. 2. Nested sampling designs (A) spatial scales o 1, 2, and 4 m at Station 9 (June 2005) where core samples were collected from 12 1-m2 quadrats, randomly placed on
either side of a 44-m long transect. Four infaunal cores (by open circles) and two sediment cores were collected within each quadrat from ripple crests, flanks, troughs + SH,
and troughs SH (infaunal core:1 core habitat 1 =4 cores quadrat 1, n= 48; sediment cores: 2 syringe cores habitat 1 = 8 syringe cores quadrat 1, n= 96). Top insert is a
digital photograph of quadrat 1 indicating core samples and habitats, (B) spatial scales o 1 m, r 60 m, r 200 m at Stations 9 and 30 (multiple dates in 1994 and 1995)
where triplicate paired crest and trough samples o1 m apart were nested within three 60-m diameter circles (substations), nested within a 200-m diameter circle at each
station. Stations 9 and 30 are 4 km apart. Large filled central circle denotes permanent station mooring, filled circle in center of substation indicates randomly located
permanent substation mooring, and ovals with circles inside represent paired crest (i.e., open) and trough (i.e., filled) samples (n= 6 cores substation 1 [3 crests, 3 troughs];
18 cores station 1) on each sampling date.
included ripple crests, flanks, troughs + SH, and troughs SH
(Fig. 2A). Separate sediment cores were also taken for grain size
and sediment analyses (i.e., carbon, nitrogen, chl a, and
pheophytin) using weighted, modified syringe cores (5.3 cm2
and 8-cm long). Sediment cores were taken as close as possible to
each infaunal core (2 syringe cores habitat 1 = 8 syringe
cores quadrat 1, n= 96), (Fig. 2A).
2.2.2. Large-scale (cm–km), multiple dates 1994–1995
A previously collected dataset originally used to provide
baseline information on the spatial and temporal distribution of
infaunal communities at LEO-15 (Grassle et al., accepted) was
examined (only Stations 9 and 30) in the present study to address
questions regarding the persistence of ripple crest and trough
community patterns across relatively large spatial scales, and over
successive sampling dates. Infaunal data in the 1994/1995 study
were highly comparable to those taken in 2005 with respect to
sampling location (LEO-15, Station 9), methods (i.e., both
employed nested designs; paired crest and trough samples;
utilization of the same diver-collected hand corers; and a 300mm mesh screen) and effort (n =9 cores habitat 1 station 1 date 1
[1994/1995] and n = 12 cores habitat 1 [2005]). Infaunal core
samples were collected on 20 July 1994, 20 September 1994,
and November/December 1994 (14 November [Station 9],
2 December [Station 30]), 5 June 1995, and 12 October 1995. At
each station a nested, partially randomized sampling design
(habitat specified: crest or trough) was used where within each
station (each station: 200-m diameter), three 60-m diameter
areas called ‘‘substations’’ were set up, and within each of these a
pair of infaunal samples including one from a crest and the other
from a trough o1 m apart, were collected at three points (6 cores
[3 crests and 3 troughs] substation 1 = 18 cores station 1; n = 180
cores over all dates sampled) (Fig. 2B). Thus, spatial scales of
interest included o1 m, r60, r200, and 4 km. Separate
sediment cores for grain size and sediment properties were not
examined in 1994/1995.
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Fig. 3. Means 795% confidence intervals, with n= 12 for (A) total density of infauna June 2005, (B) richness, (C) Shannon diversity H0 , and (D) evenness J0 . The same letters
(a, b) indicate no significant differences between habitats (p 40.05, Mann–Whitney U Test). Scales on y-axes differ among panels.
2.3. Infaunal samples
2.5. Data analysis
All infaunal samples (samples from 2005 and 1994/1995) were
sieved over a 300-mm mesh screen, fixed in 10% formalin and
seawater mixture, and then promptly transferred to 70% ethanol
with rose bengal. Infauna were identified to the lowest taxonomic
level possible (i.e., genus or species). In some cases,
small juveniles could not be identified and were grouped by
family or some higher level of classification and referred to as
spp.
Community composition was compared among habitats on
individual infaunal cores (i.e., cores were not averaged or pooled)
and separate analyses were conducted for the June 2005 data as
well as for each sampling date in 1994/1995 using Chord Distance
Normalized Expected Species Shared (CNESS) (described by
Trueblood et al., 1994). CNESS is an extension of Orlóci’s (1978)
chord distance and Grassle and Smith’s (1976) Normalized
Expected Species Shared (NESS). CNESS constructs a dissimilarity
matrix from a sample by species matrix, that depends on the
number of expected species shared in a random draw of n
individuals from two samples. This index is sensitive to rare
species as well as to abundant ones. Distribution patterns were
clustered using weighted, pair-group mean average sorting of
CNESS dissimilarities along with a metric scaling of CNESS using
COMPAH 96 and Matlab programs written by Gallagher, University of Massachusetts, Boston (http://alpha.es.umb.edu/fa
culty/edg/files/edgwebp.htm). The hypergeometric probability
matrix (H) that was produced by metric scaling of CNESS was
then examined by principal components analysis (PCA-H). The
PCA-H plot is very similar to that produced by non-metric
multidimensional scaling (NMDS) (Trueblood et al., 1994;
Snelgrove et al., 2001), but the benefit of the metric scaling is
that CNESS distances among samples are conserved and therefore
species that contributed 45% to CNESS variation among samples
can be displayed in a Gabriel Euclidean distance biplot overlay
(Gabriel, 1971). In the biplot, the length and angle of species
vectors indicate the contribution of the species to the PCA-H axes.
2.4. Sediment properties (June 2005)
Sediment grain size analysis was conducted using stacked
sieves (Z2, 1 mm, 500, 250, 125, 32, r32 mm). For analytical
purposes sediments were described as medium-to-coarse-grained
( Z250 mm) or fine-grained (o250 mm). A small amount of
sediment was removed from the top layer ( 1-cm deep) of
syringe cores taken for sediment analysis and frozen for later
determination of ambient concentrations of total carbon, nitrogen,
chlorophyll-a, and pheophytin. Sediment for carbon and nitrogen
analysis was first dried, ground, and acidified in silver cups to
remove carbonates and then measured using a Fisons NA1500N
elemental analyzer with acetanilide as a calibration standard. Cchl
a and pheophytin was extracted from sediment (3–11 g) in 90%
acetone and determined by fluorometric analysis on a Hitachi
F2000 spectrofluorometer (modified from Strickland and Parsons,
1972; APHA, 1992).
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Fig. 4. Means7 95% confidence intervals for (A, B) total density of infauna in ripple crests compared to troughs on each sampling date (20 July 1994, 20 September 1994, 14
November/2 December 1994, 5 June 1995 and 12 October 1995; n= 90) at Stations 9 and 30 respectively, (C, D) richness, (E, F) Shannon diversity H0 , and (G, H) evenness J0 .
Note scale on y-axes differs among panels.
Community measures including density of total infauna, taxon
richness, Shannon diversity H0 , and evenness J0 were also
compared among the four habitats by plotting means with 95%
confidence intervals for each sampling date and station. To
determine whether there were significant differences in any of
these measures among the four habitats examined in 2005 a
Kruskal–Wallis test was used. For significant results, post-hoc
testing was conducted using pair-wise Mann–Whitney U tests in
SPSS 10.0. A Mann–Whitney U test was also performed (pooled
across sampling dates) to determine if there were significant
differences between crests and troughs at Stations 9 and 30 in
1994/1995.
Principal components analysis (PCA) determined differences
among the four habitats based on sediment properties (June 2005
only) including sediment grain size (i.e., medium to coarser
grained Z250 mm and finer sediments o250 mm) and indirect
measures of food availability (i.e., total particulate organic carbon,
chlorophyll-a, and pheophytin) (SPSS 10.0). Values for nitrogen
were not used in this analysis since they were close to the
detection limits of the elemental analyzer. Prior to analysis,
variables were standardized to z-scores, thus weighting all
variables equally. To determine whether there were significant
differences in environmental variables among the four habitats a
Kruskal–Wallis test was conducted followed by a pair-wise Mann–
Whitney U tests.
3. Results
3.1. Community measures
In June 2005, infaunal density, richness, and diversity were
higher in ripple troughs compared with the other three habitats
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crest
trough -SH
trough +SH
0.8
flank
relative to 1994/1995, which may be related to larger scale
changes in productivity in the Mid-Atlantic Bight.
Spisula solidissima
PCA-H axis 2 (16%)
0.6
3.2. Spatial patterns
0.4
0.2
0.0
Tellina agilis
-0.2
-0.4
Oligochaeta spp.
Nemertea spp.
Acanthohaustorius sp.
-0.6
-0.8
-0.8
-0.6
-0.4
-0.2
0.0
0.2
0.4
0.6
0.8
0.8
Spisula solidissima
0.6
0.4
PCA-H axis 2 (16%)
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0.0
-0.2
4
76 1
10
85
61
5
0.2
3
8
6
9
-0.4 Nemertea spp. 11
10
-0.6
-0.8
-0.8
-0.6
-0.4
-0.2
7 10
3
7
9 9
2
2 8 Tellina agilis
1
11
312 4
5
10
6 4
2
12
8
4
7
1
11
0.0
12 Oligochaeta spp.
Acanthohaustorius sp.
2
0.2
0.4
0.6
0.8
PCA-H axis 1 (24%)
Fig. 5. PCA-H metric scaling ordination of infaunal core assemblage spatial
patterns for June 2005 at Station 9 based on CNESS (n= 5 individuals). First two
axes explain 24% and 16% of the variance in the data respectively. Solid arrows
indicate taxa contributing to 45% of CNESS variation in biplots. Taxa in bold
indicate those with heavily weighted factor loadings (7 0.5). (A) Individual cores
are labeled according to habitat and by stippling/shading (for illustration purposes
only), (B) quadrat (numbers correspond to those used in the sampling design
shown in Fig. 2).
(Figs. 3A–C). Kruskal–Wallis tests showed significant difference
among these habitats only for infaunal density (p= 0.035, n =48).
Pair-wise post-hoc tests indicated that density in troughs SH
was significantly different compared with flanks (p= 0.003, n =24).
Evenness values were similar across habitats (Fig. 3D).
Infaunal density and richness were also consistently higher in
troughs compared to crests at Stations 9 and 30 on all dates
sampled (exception =richness in October 1995) (Figs. 4A–D),
however this difference was only significant for density (Station
9: p= 0.027, n = 90; Station 30: p =0.004, n = 90). Infaunal diversity
showed the opposite trend to that observed for June 2005 with
higher diversity in crests compared to troughs for the majority of
sampling dates (Figs. 4E, F) (Station 9: 0.030, n =90; Station 30:
0.012, n = 90). Evenness was also generally higher in crests than in
troughs (Figs. 4G, H) (Station 30: p= 0.006; n =90). Overall, a total
of 709 individuals were collected in June 2005 (n =48)
encompassing 35 different taxa, whereas a total of 43,708
individuals were collected encompassing 140 different taxa in
1994/1995 (n = 180). Moreover, density and richness were much
lower in June 2005 (n = 12) compared to June 1995 (n =9) (Figs. 3
and 4). Scuba divers at the study sites have also noticed reduced
densities of epifaunal species at the study site in recent years
PCA-H analysis of infaunal cores from June 2005 indicated that
samples clustered together by habitat type (i.e., crests, flanks, and
troughs [ +SH and SH]) rather than with respect to spatial
arrangement along the transect (i.e., by quadrat) (Figs. 5A, B).
Thus, samples collected close together (paired crest and trough
cores taken o1 m apart) were more different from each other
than samples from the same habitat type taken further apart at
distances of 2–44 m (see Figs. 2A and 5A). At relatively larger
scales, samples also generally grouped by habitat type in July 1994
(Station 30), September 1994, November/December 1994, and
June 1995 (Figs. 6A–D). Clustering of cores based on habitat type,
however, did not hold for samples taken in July 1994 (Station 9) or
in October 1995 where paired crest and trough samples grouped
together by station (Figs. 6A, E).
In June 2005 five taxa were identified in Gabriel biplots as
being important (contributing to 45% of CNESS variation) in
distinguishing among the habitat groupings including the bivalves
Spisula solidissima and Tellina agilis, the amphipod Acanthohaustorius sp., Nemertea spp., and Oligochaeta spp. (Fig. 5A, Table 1).
Densities of species with high factor loading scores ( 70.5)
significantly differed among the four habitats (Kruskal–Wallis
test) including S. solidissima (p = 0.023, n =48; highest in troughs
SH/+ SH), T. agilis (p= 0.039, n = 48; lowest in crests) and
Nemertea spp. (p =0.035, n =48; highest in crests) (see Fig. 7 for
pair-wise post-hoc comparisons). Depending on the date
examined in 1994/1995, different combinations of 13 taxa (i.e., 8
polychaetes, 3 bivalves, Oligochaeta spp., and Nemertea spp.)
were important in distinguishing among habitat and station
groupings (3–6 taxa per date) (Table 1). Most taxa (7 out of 13)
were important in distinguishing among groups on a single date,
however S. solidissima and Nemertea spp., which were important
in distinguishing among habitats in June 2005, were also
important on three of the five dates examined in 1994/1995
(Fig. 7, Table 1). Moreover, the polychaete Polygordius jouinae was
important on four dates in 1994/1995. Densities of P. jouinae and
Tharyx acutus were consistently higher in troughs compared to
crests, whereas density of Nemertea spp. was consistently higher
in crests. Density of S. solidissima was highly variable between
crests and troughs depending on station and date. Species with
significant differences in density between crests and troughs at
either Station 9 or 30 are given in Table 2.
3.3. Habitat related sediment properties (June 2005)
Spatial patterns based on PCA analysis of sediment properties
showed similar clustering of samples based on habitat type to
those observed for the infaunal data (Fig. 8). Samples taken from
ripple crests were the most distinct, trough samples ( + SH and
SH) formed another group, and samples from ripple flanks
overlapped considerably with those from crests and troughs.
Principal components axis 1 was important in distinguishing
among the habitat groupings described above and explained 45%
of the variation in the data. Variation among samples within
habitats generally occurred along axis 2 and explained 32% of
variation in the data. A comparison of sediment properties among
habitats significantly differed for coarse and fine-grained
sediment (p = o0.0001, n= 43; p = o0.0001, n = 43) respectively,
as well as sedimentary organic carbon (p = o0.0001, n = 48) (see
Fig. 9 for pair-wise post-hoc comparisons). Generally crests
contained coarser sediments ( Z250 mm) and higher amounts of
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Fig. 6. PCA-H metric scaling ordination of infaunal core assemblage spatial patterns for each date sampled in 1994/1995 at Stations 9 and 30 based on CNESS (n= 10
individuals). First two axes explain 27–37% and 17–21% of the variance respectively depending on sampling date. Solid arrows indicate taxa contributing to 45% of CNESS
variation in biplots. Taxa in bold indicate those with heavily weighted factor loadings ( 7 0.5). Individual cores labeled according to station and habitat from which they
were collected. Sample groupings discussed, indicated by shading (highlight habitats) and dashed lines (highlight stations), (for illustration purposes only).
Table 1
Summary of 15 taxa/species contributing to 45% of CNESS variation among samples and displayed in Gabriel Euclidean distance biplots.
Group
Taxa/species
Polychaeta
Polygordius jouinae
Tharyx acutus
Tharyx kirkegaardi
Syllides convoluta
Aricidea catherinae
Caulleriella sp. A
Spionidae juv. sp. A
Bivalvia
Oligochaeta
Spisula solidissima
Nucula annulata
Tellina agilis
Peosidrilus spp.
Oligochaeta spp.
9 June
2005
20 July
1994
+
+
+
+
20 September
1994
14 November/
2 December 1994
5 June
1995
12 October
1995
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
Nemertea
Nemertea spp.
Nemertea sp. A
+
Amphipoda
Acanthohaustorius sp.
+
+
+
+
+
+
+ Indicates taxon contributed to variation on a particular sampling date (i.e., June 2005, July 1994, September 1994, November/December 1994, June 1995 and October
1995).
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Fig. 7. Mean densities 7 95% confidence intervals of taxa contributing to 45% of
CNESS variation in Gabriel biplots with heavily weighted factor loadings ( 7 0.5)
(n= 12) for samples taken June 2005. Same letters (a, b) indicate no significant
differences in density between habitats (p 40.05, Mann–Whitney U Test).
sediment chl a (i.e., benthic diatoms), whereas a greater
proportion of finer sediments ( o250 mm), particulate organic
carbon, and pheophytin were present in troughs ( SH and + SH).
4. Discussion
Crests, troughs (including areas with and without shell hash),
and to a lesser extent flanks of sand ripples were instrumental in
identifying infaunal community patterns in highly mobile, wellsorted continental shelf sediments over scales of centimeters to
kilometers on the majority of sampling dates examined. Infaunal
samples primarily grouped by habitat type rather than spatial
arrangement of the sampling design(s) (e.g., groups did not cluster
by quadrat, substation etc.). Habitat-based community patterns
varied at scales o1–200 m on most dates, with less variability at
the between-station scale (4 km) on three of the five dates
examined. Habitat-defined communities at the smallest scale
examined ( o1-m2) in ripple crests, troughs, and/or flanks were
more different from each other than communities within either
2229
crest, trough, or flank habitats 2m–4 km apart. In concert with our
findings, Barros et al. (2004) also found less variability in infaunal
communities (500-mm sieve; family level identification) from
replicate to replicate within crests and within troughs than
between crests and troughs (scales of r4–10 m) in Botany Bay,
Australia at 7–8 m depth.
Abundances of infauna inhabiting crests have been described
as different from those in troughs in high-energy subtidal (e.g.,
nematodes: Sameoto, 1969; macrofauna 500-mm sieve: Barros
et al., 2004) and intertidal sandy sediments (crustaceans: Grant,
1981) with some having significantly higher abundances in
troughs than crests (Barros et al., 2004) and vice versa (Grant,
1981). In the present study, various combinations of taxa
characterized the patterns described depending on sampling date.
Given the diversity of reproductive strategies, feeding modes, food
preferences, and motility of infaunal organisms, it is not
surprising that different taxa exhibit different habitat associations
and patterns. Community differences between ripple crests and
troughs on the majority of dates, irrespective of station, were
driven by differences in the relative abundance of three taxa: the
deposit-feeding polychaete P. jouinae, the suspension-feeding
surfclam S. solidissima, and predatory Nemerteans. Overall,
infaunal density and species richness were consistently higher
in troughs compared to crests. Qualitative observations by divers
indicate lower densities of certain macrofauna (e.g., Echinarachnius parma, Cerianthiopsis americanus) in recent years compared to
1994/1995. Such changes may be linked to declines in the
magnitude of the fall and winter phytoplankton blooms (Schofield
et al., 2008) which in turn are likely to affect the level of
particulate matter reaching the bottom.
We found evidence for differences in food resources associated
with crests and troughs of ripples. Ripple troughs contained
significantly higher levels of particulate organic carbon ( 1.2
times higher) associated with finer sediments, compared with
crests and flanks. Chl a and pheophytin concentrations were major
factors in determining within-habitat variability. Although concentrations in June 2005 did not differ substantially among
habitats in the present study, Ramey and Bodnar (2008) found
concentrations up to five times higher in ripple troughs than
crests at Station 9 and Node B following the spring phytoplankton
bloom (i.e., in May 2006). Topography of sandy rippled beds
creates pressure-driven transport of water through the interstices
of the sediments augmenting the deposition, transport, and
patchiness of organic matter in permeable shelf sands (Huettel
et al., 1996; Pilditch et al., 1998; Precht and Huettel, 2003; Reimers
et al., 2004). In oscillatory flows such as those found at the study
site, ripples as small as 0.7-cm high (3-cm wavelength) can
enhance pore–water exchange rates by factors of 6–15 (Precht and
Huettel, 2003). Organic matter may also accumulate in troughs by
settling there as a result of reduced shear stress. Current speeds,
direction, and topography at the study area, can change on time
scales from seconds to seasons (e.g., Traykovski et al., 1999)
creating patchy distributions of food resources.
Patchiness of resources coupled with the behavior of species
can determine the distribution of individuals within communities
(Thrush et al., 1989), and the heterogeneity generated by
topographic features may be an important source of microhabitat
specialization and resource partitioning (Hogue and Miller, 1981;
Ramey and Bodnar, 2008). Several studies have suggested that
active selection by post-larval stages may also be responsible for
distribution patterns associated with crests and troughs (e.g.,
Sameoto, 1969; Grant, 1981). Flume experiments have shown that
under realistic flows at the study site (free stream velocity of
5 cm s 1; u* =0.32 cm s 1; Styles, 1998) and flat bed conditions,
adult P. jouinae selected for higher levels of particulate organic
matter, and the worms can potentially traverse the wavelength of
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P.A. Ramey et al. / Continental Shelf Research 29 (2009) 2222–2233
Table 2
Mean density with 95% confidence intervals for taxa contributing to 45% of CNESS variation among samples and displayed in Gabriel Euclidean distance biplots for each
sampling date at Stations 9 and 30 (i.e., July 1994, September 1994, November/December 1994, and June 1995).
Date
20 July 1994
Species
Polygordius
jouinae
Tharyx acutus
Syllides
convoluta
Spisula
solidissima
Station 9
Station 30
Crest (no. ind.
38.5 cm 2)
Trough (no. ind.
38.5 cm 2)
Mann U, p-value
n= 18
Crest (no. ind.
38.5 cm 2)
Trough (no. ind.
38.5 cm 2)
Mann U, p-value
n= 18
0.00
26.447 13.8
10.0 (0.006)
0.0
0.11 7 0.3
1.567 1.7
0.3370.5
2.22 7 1.9
0.447 0.58
0.89 7 0.8
10.78 7 6.6
4.117 2.4
0.677 0.9
16.0 (0.031)
10.0 (0.006)
10.78 7 4.0
7.677 3.2
2.44 71.1
0.89 70.5
17.5 (0.040)
20 September 1994
Spisula
solidissima
17.117 9.1
39.67716.0
13.0 (0.014)
5.567 3.19
7.78 7 4.6
4.5 (o0.001)
14 November/2
December 1994
Polygordius
jouinae
Spionidae juv.
sp. A
46.44 7 26.6
146.67741.7
7.0 (0.002)
46.337 30.35
381.88 7 206.3
15.5 (0.046)
0.0
0.0
13.78 7 17.9
37.007 60.4
93.33764.9
23.78 7 25.3
360.22 7 230.5
8.677 3.67
9.007 8.91
11.56 7 6.1
21.227 18.81
5 June 1995
Polygordius
19.677 17.8
jouinae
Nemertea sp. A 6.337 2.7
Tellina agilis
0.30 70.32
2.667 1.49
1.22 7 0.63
17.0 (0.036)
18.0 (0.032)
13.0 (0.015)
Mann–Whitney test for differences in density between crest and trough habitats at a =0.05 are also given. Only species and corresponding dates with significant differences
in density are listed. Mann–Whitney U values are followed by p-values in parentheses.
Fig. 8. (A) Spatial patterns defined by principal components analysis (PCA) of sediment properties. First two axes explain 45% and 32% of variance in data respectively.
Individual cores labeled according to (A) habitat and by stippling/shading (for illustration purposes only), (B) Plot of factor loadings for each environmental variable. Heavily
weighted loadings (70.5) are bolded.
a typical ripple (14–30 cm) in 35–75 min (Ramey, 2008; Ramey
and Bodnar, 2008).
Infauna may also be passively transported to (via re-suspension and bedload transport) and deposited in troughs (Eckman,
1979). There is also some evidence for larval and/or post-larval
selection, and passive or active transport via re-suspension of
bedload by P. jouinae and juvenile S. solidissima at the study site
(Snelgrove et al., 1999). Inconsistent distribution patterns of
S. solidissima in crests and troughs may have resulted from
differences in susceptibility of individuals to re-suspension or
bedload transport. The need for this suspension-feeding clam to
remain in sediments with relatively higher levels of sedimentary
organic matter is probably much less important than for a deposit
feeder like P. jouinae. Moreover, juvenile S. solidissima are
restricted to surface sediments due to their short siphon length
(Zwarts and Wanink, 1989) which makes them susceptible to re-
suspension and bedload transport as well as predation.
A combination of these factors is likely to influence distributions
of infauna between crests and troughs. The consistency and
repeatability with which these small-scale species distributions
occurred in this study, suggest that they are quickly re-established
following sediment re-suspension and ripple migration.
Differences in ripple characteristics such as height and
wavelength may also be related to the spatial variability of
infauna and finer scale patchiness in organic matter distribution
in sandy continental shelf sediments. In Botany Bay, Australia
Barros et al. (2004) found some evidence for a relationship
between spatial variability of infaunal assemblages (500-mm
sieve; family level identification) and the size of ripples, where
dissimilarity between replicates (within crests and within
troughs) and the dissimilarity among replicates (crests and
troughs) were greater for larger ripples. Video and still images
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a
b
b
25
b
a
b
Flank
120
Crest
P.A. Ramey et al. / Continental Shelf Research 29 (2009) 2222–2233
2231
bc
c
100
Fines (%)
80
15
10
5
60
a
b
0.03
0.02
0.01
0.00
8.0e-4
6.0e-4
4.0e-4
2.0e-4
0.0
3.5e-4
3.0e-4
Chl a (mg g-1)
1.0e-3
b
Trough -SH
a
Pheophytin (mg g-1)
Carbon (%)
0.04
0
Trough +SH
Coarse (%)
20
Habitat
2.5e-4
2.0e-4
1.5e-4
1.0e-4
5.0e-5
Trough -SH
Trough +SH
Flank
Crest
0.0
Habitat
Fig. 9. Means 7SD for sediment properties, with n= 10–12 (A) medium–to-coarse grained (Z 250), (B) fines (grain sizes o 250 mm), (C) carbon, (D) pheophytin and (E)
chlorophyll-a. Same letters (a, b) indicate no significant differences in concentration between habitats (p 40.05, Mann–Whitney U Test). Scales on y-axes differ among
panels.
taken along our study transect in 2005 indicated considerable
variability in ripple morphology with ripple heights ranging from
5 to 15 cm. Some ripples were high, symmetrical, and with sharp
crests, whereas others were lower, in a bed that was irregular and
hummocky. These heights are comparable to those measured
during a particularly active period from August to September 1995
at our study site (heights: 3–15 cm; wavelengths: 10–100 cm),
where mean alongshore currents (measured 44 cm above the
bottom) near Station 9 were 5–20 cm s–1 and cross-shore currents
associated with the tides were generally r8 cm s–1 (Traykovski
et al., 1999).
Although habitat groupings in the present study were not well
separated from each other in ‘‘PCA space’’ this is understandable
since species differences among habitats were generally related to
differences in density rather than species presence in, or absence
from, a particular habitat. Moreover, habitats were close to each
other, in a highly dynamic environment with no obvious barrier to
species dispersal. Similarity in communities in troughs + SH and
troughs SH was likely due to the fact that shell hash was present
in relatively small quantities and consisted of small shell
fragments rather than large surfclam valves, which also occur as
transient features (Able et al., 2003). Shell hash was hypothesized
to provide a different habitat because its presence affects the
hydrodynamic regime in the surrounding sediments (i.e., velocity
and turbulence of the benthic boundary layer; Newby, 2006), and
it may also provide areas of refuge from predators (Kamenos et al.,
2004).
The only dates where communities did not differ between
crests and troughs were in July 1994 (Station 9 only) and October
1995. Community differences on these dates were attributed to
the largest spatial scale (4 km), i.e., between the inshore and
offshore stations, and the sampling dates corresponded with
seasons when larval recruitment for certain infaunal species is
maximal (Ma and Grassle, 2004). Thus, community differences
between the inshore and offshore station may have been a result
of factors such as circulation patterns, upwelling and downwelling
events, combined with differences in life history strategies, all of
which can differentially influence larval supply and settlement at
these two locations (Ramey, 2008; Ma, 2005; Ma et al., 2006;
Snelgrove et al., 1999; Snelgrove et al., 2001; Weissberger and
Grassle, 2003). Moreover, the October 1995 sample collection
followed a particularly stormy, two-week period at the end of
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P.A. Ramey et al. / Continental Shelf Research 29 (2009) 2222–2233
September. Thus, stormy conditions may have resulted in
substantial sediment re-suspension and transport, disrupting the
community patterns established in crests and troughs during
calmer periods.
This study highlights the influence small-scale differences in
habitat can have on the distribution and concentration of
sedimentary food resources and infaunal species distributions,
abundances, and related community measures even in relatively
homogeneous, mobile shelf sediments. Several individual taxa
showed significantly greater densities in either crests or troughs
of sand ripples. Infaunal density and species richness were higher
in ripple troughs compared to crests, whereas diversity showed
the opposite pattern on the majority of dates examined. A priori
knowledge of whether a benthic sample came from a crest or
trough helped to explain some of the small-scale infaunal
patchiness observed in relatively homogeneous, well-sorted
sandy sediments. Ubiquitous and persistent features such as
crests and troughs of sand ripples should be considered in future
sampling designs when examining infaunal community patterns
as they may help identify the scales over which particular
processes and mechanisms are important, and aid in the design
of experimental studies.
Acknowledgements
Special thanks to Char Fuller, and the Rutgers Institute of
Marine and Coastal Sciences (IMCS) dive team for collecting the
infaunal cores at the LEO-15 research site; Kenneth Elgersma for
his help on the boat and fixing samples; to Kate Douglas and Tiara
Johnson for their assistance in sorting samples in the laboratory;
Carola Noji and two anonymous reviewers provided constructive
comments on the manuscript. P.A. Ramey was supported by an
IMCS graduate assistantship and graduate student research funds
from the Rutgers University Marine Field Station, New Jersey. This
is contribution 2009-6 from IMCS.
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