Limnol. Oceanogr., 34(7), 1989, 1247-1262
0 1989, by the American
Society of Limnology
and Oceanography,
Inc.
Vertical distributions of the epifauna on manganese nodules:
Implications for settlement and feeding
Lauren S. Mullineaux 1
Scripps Institution of Oceanography, University of California, San Diego, La Jolla 92093
Abstract
Over 65% of the sessile organisms living on manganese nodules from the tropical North Pacific
belong to taxa whose abundances are related to vertical position on the nodule. The nodule surface
texture and boundary layer flow environment, two factors that also vary vertically, were investigated
to determine whether they could account for the observed faunal distributions. The surface texture
of nodules from the tropical Pacific is generally rough and knobby at the nodule base and smooth
near the summit. Twenty-five taxa, including 68% of the total individuals, were found in significantly different abundances between the rough and smooth surfaces of 34 nodules. These distributions may be due to larval responses to surface texture and can account for much of the observed
vertical zonation of the fauna. Boundary layer flows over nodules were characterized from laboratory flume studies and field observations. In flows at the field site, it is expected that mean
boundary shear stress and horizontal flux of particles (food or larvae) will increase from the nodule
base to the summit, while particle contact rate and deposition will decrease. The observations that
suspension feeders persist near the nodule summit and deposit feeders concentrate near the base
suggest that vertical distributions of some taxa may be determined by adult feeding requirements.
Individuals of most taxa are relatively scarce at the nodule base, indicating that their larvae are
not colonizing where they accumulate passively. High abundances of matlike agglutinated foraminifers (of unknown feeding type) at the nodule summit may be due to larval responses to the
relatively‘higher shear stresses.- -
tributions expected from feeding and settlement responses to flow and surface texture.
The study concentrates on these specific
processes because they are important in
shallow-water habitats and because they can
be investigated without extensive in situ
measurements.
The influence of flow on benthic marine
invertebrates has received much recent attention (see Jumars and Nowell 1984; Butman 1987). In particular, researchers have
focused flow-related studies on suspension
feeding (LaBarbera 1984; Merz 1984; Sel Present address: Woods Hole Oceanographic Inbens
and Koehl 1984; Holland et al. 1986;
stitution,
Woods
Hole,
Massachusetts
02543.
-’
Muschenheim
1987), deposit feeding
Acknowledgments
(Taghon et al. 1980; Miller and Jumars 1986)
This work was supported by a NSF predoctoral fellowship to L.S.M., by ONR grant NOOO14-89-J-1112 and larval settlement (e.g. Eckman 1983;
to C.A. Butman and L.S.M., by NOAA contract 83- Rittschof et al. 1984; Kern and Taghon
SAC-00659 to R. Hessler, and by the Coastal Research
1986). Most of these studies have concenCenter at Woods Hole Oceanographic Institution.
trated on shallow-water habitats, but deepContribution 6947 from Woods Hole Oceanographic
Institution.
water communities are also likely to be
The opportunity to participate in a deep-sea field
strongly influenced by near-bottom curprogram was provided by J. Snider and R. R. Hessler.
rents.
For instance, physical disturbance
Helpful suggestions for data collection and analysis
caused
by benthic “storms” may control the
were made by J. T. Enright, A. Genin, and W. M.
Smithey. P. A. Jumars and A. R. M. Nowell made species composition and spatial distribuavailable the flume facilities at Friday Harbor Labotions of benthic fauna at a deep-water site
ratories, and D. C. Miller and J. E. Eckman contributed
in the North Atlantic (Thistle et al. 1985)
technical assistance.This manuscript has benefited from
and currents may determine the distribucomments by C. A. Butman, R. R. Hessler, N. D.
Holland, P. A. Jumars, D. L. Penry, and three anon- tions of some suspension feeders on seaymous reviewers.
mounts (Genin et al. 1986). Flumes have
1247
A diverse group of epifaunal invertebrates, dominated by agglutinated foraminifers, encrusts the surface of abyssal manganesenodules (Mullineaux 1987). A variety
of approaches is necessary to investigate
processes structuring these epifaunal communities, since experimental work is limited by the inaccessbility of most nodule
habitats. The present study compares observed distributions of epifaunal taxa to dis-
1248
Mullineaux
proven valuable in modeling near-bottom
environments and are particularly useful for
simulating wave-free, flat seabeds, such as
abyssal plains.
Plume studies of flows around hemispheres (which approximate the shape of
nodules on the seafloor) have shown that
flow accelerates over the top of the object,
and eddies form downstream from a separation point in a wide range of flow conditions (Brayshaw et al. 1983; Schlichting
1936, figure 22; Hunt et al. 1978). In turbulent flow, Paola (1983) found that the
boundary shear stress (a measure of the drag
force exerted on the bottom by the nearbottom flow) under eddies in the wake of a
hemisphere is low, making the eddies a
probable site of deposition. Comparable
flume studies were conducted in the present
study in flow regimes similar to abyssal nodule fields in order to determine particle fluxes, contact rates, and deposition onto nodules in unidirectional flows. When this
information is extended to flows with tidal
and longer period fluctuations, predictions
of larval settlement patterns on abyssal nodules and of food fluxes over and onto them
can be made.
Surface texture may also be a factor in
structuring communities on nodules. Nodule surface texture tends to be rougher near
the base than near the summit (illustrated
in figure 8 of Sorem et al. 1979). The difference between smooth nodule surfaces
(composed of tightly packed, grapelike clusters of tiny spheroids, called botryoids) and
rough nodule surfaces (composed of botryoids clustered into larger protruding knobs)
is probably large enough to be detected tactilely by deep-sea invertebrate larvae. Since
surface texture is known to influence settlement of larvae (Crisp and Barnes 1954;
Barnes 1956) and spores (Christie 1973),
vertical distribution patterns of encrusting
adults may be due to larval responses to
surface texture. If particles accumulate on
rough surfaces, texture may also influence
epifaunal distributions by enhancing food
availability for deposit feeders.
The approach used here is to predict distributions of organisms on nodules (based
on physical features such as surface texture
or particle transport) and compare them with
observed distributions of individual taxa
and taxa grouped by feeding type. The first
three alternative hypotheses address larval
settlement: larvae of nodule epifauna settle passively and adults will be most abundant at the nodule base where larvae contact
the nodule surface most frequently; larvae
settle as an active response to boundary shear
stressand abundances of individual taxa will
correlate positively or negatively with shear
stress, depending on the response of that
particular taxon; and larvae settle in an active response to small-scale surface texture
on the nodule.
The use of adult distributions to test the
settlement hypotheses rests on the assumption that settlement patterns persist in adult
distributions. This assumption may or may
not be appropriate for this community of
organisms, so two additional hypotheses
addressing the feeding requirements of
adults in relation to flow-mediated particle
fluxes are considered: suspension-feeding
taxa persist where horizontal particulate flux
is relatively high; and deposit-feeding taxa
persist where particle deposition is relatively high.
Field site
Manganese nodules were collected with a
0.25-m2 box core (earlier version described
by Hessler and Jumars 1974) in the tropical
North Pacific at a depth of 4,500 m. The
site is at l5”N, 125”W, between the Clipperton and Clarion fracture zones near Deep
Ocean Mining Experimental Survey Site C
(Bischoff and Piper 1979). The sediments,
siliceous pelagic clays, are well below the
carbonate compensation depth (CCD).
Bottom temperatures at this site are low
(1.4”C) and relatively constant. Organic input to the site is controlled by primary productivity at the surface, which averages 120
mg C m2 d-l in summer (El-Sayed and Taguchi 1979). This surface productivity contributes to the relatively high abundance of
sediment-dwelling macrofaunal organisms
(>300 pm), which attain densities of up to
155 individuals per 0.25 m2 with a mean of
89 (Wilson and Hessler unpubl. rep.).
Bottom currents near the study site were
monitored in 1977 for 6 months with a vertical array of current meters (Hayes 1979).
1249
Epifaunal distributions on nodules
Current velocities oscillated on tidal (semidiurnal) and inertial (47.6 h) time scales,
but long-period (>48 h) oscillations dominated. Tidal rotation was nearly symmetrical, with only a slight mean trend to the
northwest. Current speeds measured 6 m
above the seafloor ranged from 0 to 12 cm
s-l and averaged 6. Velocities reached a
maximum at 30 m above the bottom, in a
pattern consistent with previous currentmeter studies at nearby sites (Amos et al.
unpubl. rep.; Harvey and Patzert 1976).
Temperature profiles indicated weak stratification in the bottom 200 m and no obviously mixed benthic boundary layer (such
as those described on the Hatteras abyssal
plain by Armi and Millard 1976) could be
detected.
The near-bottom velocity gradient over
an abyssal nodule field is influenced both
by current velocities above the boundary
layer and by the topography of the seafloor.
It can be characterized by us, the boundary
shear velocity, assuming steady unidirectional flow and an absence of nearby topographic features. Calcuations of u* for field
flows are often made by measuring velocity
profiles in the logarithmic layer of the
boundary layer (Chriss and Caldwell 1982;
Gross and Nowell 1983; Gross et al. 1986).
If a profile is not available, however, the
velocity at a single height within the logarithmic layer can be used to estimate u* less
precisely:
u,
=
(U*/K)h(Z/Zo)
(1)
where U, is the current velocity at height z,
K is von Karman’S
Constant
(0.4), and z. is
bottom roughness. This estimate of us ‘is
constrained because it must correspond to
a relatively narrow range in bottom drag
coefficient (Cd, Sternberg 1968).
Bottom roughness can be estimated from
the height (h) and areal cover (X) of “roughness elements” on a surface (Lettau 1969):
Table 1. Comparison between boundary layer flows
in the tropical North Pacific study site and the laboratory flumes. Areal cover (X) and bottom roughness
(zJ, presented as range (mean), were calculated from
photographs of 12 box cores taken at the study site.
Nodule height (h) was measured from eight nodules
chosen at random from each core. Mean velocity (U)
at 600 cm above the seafloor was measured by Hayes
(1979) with a current meter deployed for 6 months
near the study site. Calculations of field shear velocity
(u,J are explained in the text. In the flume, U* was
calculated from vertical velocity profiles taken over
nodules 2.0 m downstream from the first nodule in a
2.5-m-long array.
North
h (cm)
x (%)
z. (cm)
U-f (cm s-l)
u* (cm s-l)
t Measured
Pacific
1.2-2.2 (1.5)
26-50 (41)
0.16-0.52 (0.31)
O-12 (6)
O-O.68
600 cm above seafloor;
Flume
1.5
6,20,46
0.05, 0.16, 0.37
1.1, 3.4,4.5
0.23,0.38, 0.69
7 cm above flume.
lineaux 1987), ranged from 26 to 52% of
the seafloor. The heights of nodules above
the sediment-water interface, measured in
a random subsample (eight nodules) from
each core, ranged from < 1 cm to >2. Ranges
for X, h, and z. at the deep-sea study site
are presented in Table 1.
Calculations of u* for the study site can
therefore be made from current velocities
recorded 6 m above the bottom (Hayes
1979) during the times when the logarithmic portion of the boundary layer was at
least 6 m thick. The thickness of a deep-sea
boundary layer scales with inertial forces
and can be estimated from the equation
(Armi and Millard 1976)
6 = ou+/f
(3)
wherefis 2 o sin (lat). At 15”N, f= 3.8 x
1Oe5s-l. If the logarithmic layer is estimated
as a tenth the height of the boundary layer
(following Gross et al. 1986), then the log
layer is at least 6 m thick for values of u*
> 0.5 cm s-l. Equation 1 can be used to
show
that current velocities (at 6 m) of 10
zo = 0.53Xh.
(2) cm s-l and greater are fast enough to form
Paola ( 1983) found that this empirical es- a log layer 6 m thick. Thus, a maximal curtimate for bottom roughness was appropri- rent velocity of 12 cm s-l sets up a maximal
ate for hemispheres in flow conditions sim- u* for the site of 0.68 cm s-l. Similarly, a
ilar to those at the field site. Areal cover of mean u* of 0.32 cm s-l can be calculated
nodules, calculated from digitized images of from the mean current velocity of 6 cm s-l
12 box cores collected at the study site (Mul- at 6 m, but is probably an overestimate since
1250
Mullineaux
the current meter may not have been within
the log layer in these flow conditions.
Row velocities (1.1, 3.4, and 4.5 cm s-l at
7 cm above the bottom) were used to generate a range of flow conditions dynamically
Methods
similar to those found at the Pacific field
Laboratory flume measurements -Two
site (Table 1).
different flumes were used to study flow acBoundary shear velocity (u*) was calcucelerations and eddies over nodulelike ob- latcd for the flume experiments from Eq. 1
jects in flow conditions similar in u* and z. with velocity measurements in the logarithto those observed at the abyssal field site. mic layer. The slope of the line from a plot
Preliminary flow and particle accumulation
of U, vs. 111 (z) resulted in reliable estimates
measurements were made in a flow-through
for z&/K (with a minimum of nine measureseawater flume (2.5 m long by 0.5 m wide) ments and an R2 > 0.96 the error was < 18%;
fitted with a 190-liter constant-head tank calculated as by Gross and Nowell 1983).
(described by Nowell et al. 198 1). These
Plow patterns around nodules in the armeasurements suggested that vertical gra- rays were visualized by injecting neutrally
dients in flow velocity and particle accu- buoyant fluorescein dye upstream of nodmulation were generated over arrays of nod- ules in a cross-stream grid pattern. The verules in simulated deep-sea flow conditions.
tical extent of eddies formed around the
Subsequent experiments, including those nodules was measured by inserting a thin
presented here, were conducted in the 17-m ruler parallel to flow in the far side of the
flume at Woods Hole (17 m long by 0.6 m flume and sighting past the eddy onto the
wide; described by Butman and Chapman ruler. The heights of attachment and sepa1989), which accommodated much longer ration points of eddies were estimated from
(2.5 m) arrays of nodules. Water depth was an average of four sightings.
The accumulation rate of particles onto
maintained at 12 cm and vertical profiles
of horizontal flow velocities were measured nodules covered with adhesive was meawith a two-axis laser Doppler velocimeter sured in order to model contact rates (de(LDV). The leading edge of the nodule array position with no erosion) of passive larvae.
was 10 m downstream from the flume inlet, Silt particles (< 63 pm) from Sippewissett
and velocity measurements were made 2 m Marsh were chosen so that their settling vedownstream from the array’s leading edge locities (w, < 0.22 cm s-l; calculated for
where the boundary layer was considered to quartz from Stokes’ equation) were similar
be fully developed because it lacked down- to those reported for benthic larvae (w, =
stream gradients in shear stress (see Paola 0.13-0.30 cm s-l for Streblospio larvae,
Hannan 1984; w, = 0.08-0.10 cm s-l for
1985).
Sizes, shapes, and spacings of nodule Capitella larvae, Butman et al. 1988).
mimics were adjusted to simulate the range The nodule mimics were made sticky by
in bottom roughnesses found at the tropical covering them with a thin film of Dow
North Pacific abyssal nodule field. These Corning Heat Sink compound. This commimics were radially symmetric, flattened pound was chosen over several other nathemispheres (1.5 cm high, 5.0-cm diam) ural and manmade adhesives because it reformed from plaster to approximate the av- tained virtually all particles (once they
erage size and shape of the exposed portion adhered) over a wide range of temperatures
of a nodule. Preliminary experiments with and even under very energetic flow condiexact casts of nodules showed that the small- tions. It should be noted, however, that neiscale textural variation and topographic ir- ther this compound nor any other adhesive
regularities did not greatly alter the size, tested traps all particles that initially contact
shape, or position of eddies around the nod- it. They trap more efficiently on horizontal
ule models. About 80 nodule mimics were surfaces than on vertical ones.
A 350”ml volume of the Sippewissett
arranged in hexagonally packed arrays so
that each model was equidistant from its Marsh silt (passed through a 63-pm sieve)
neighbors. Three arrays with different areal was mixed into suspension with a blender,
coverage of nodules (6, 20, 46%) and three then introduced into the flume 9 m down-
Epifaunal distributions on nodules
stream from the inlet and allowed to flow
over the nodule array. Particles moving
along the bottom of the flume (bedload) were
trapped 50 cm upstream of the array with
a 1-cm-high sill. Particle accumulation patterns were quantified with a dissecting microscope (30 x ) equipped with a counting
grid in one ocular. Particles were counted
on three nodules, -2 m downstream from
the array’s leading edge. On each nodule,
24 quadrats (0.64 mm2) were examined;
eight at each of three heights (0.5, 1.O, and
1.25 cm above the bottom). These eight
quadrats were spaced radially around the
nodule at 22.5” intervals. Individual particles as small as 10 pm could be seen and
counted. Accumulation experiments were
run at the same three shear velocities (0.23,
0.38, and 0.69 cm s-l) as the flow visualizations. The flume was drained and cleaned
between each run.
Epifaunal distributions - Data on the positions of organisms were collected by projecting an image of the nodule surface
through a camera lucida (mounted on a Wild
M-5 microscope) onto a Houston Instruments digitizing pad. For each organism
identified (taxonomic procedures explained
by Mullineaux 1987), records were made of
the organism’s area and location (using a
polar coordinate system centered at the
nodule summit) as well as the nodule’s surface texture (rough or smooth) at that point.
The digitized (plan-view) area of the nodule underestimates the real surface area of
a domed nodule. In order to quantify the
number of individuals per nodule surface
area (A), I added a curvature correction to
the digitized area of the nodule (Aplan):
A = Aplan+ nh2
(4)
where h is the height of the nodule above
the sediment-water interface. Densities of
organisms at 0.5-cm intervals from the nodule summit were calculated by partitioning
the surface of the nodule into concentric
rings. The area of a ring at distance r from
the summit (a,) was calculated by subtracting the area of a circle enclosed by the inner
perimeter of the ring (Ar& from the circle
enclosed by its outer perimeter (A,):
a, = A, - Ar-o.5.
(5)
1251
Areas of circles were digitized plan views
corrected for curvature as in Eq. 4 with the
height above the base of the ring (h,).
This method results in a small correction
in the inner rings and a larger correction in
the outer rings where the bias of a top view
is greatest. Organisms were assigned to the
appropriate ring according to their position
relative to the summit. Since individual organisms were small relative to the size of
the nodule, curvature corrections were not
applied to their areas. The proximity to the
summit is a good indicator of the vertical
position of an organism on a radially symmetric nodule. On the outer rings of an ellipsoidal nodule, however, organisms at an
equivalent radius along the long nodule axis
may be higher than those along the short
nodule axis. In these cases,the position relative to the nodule base is a better indicator
of an organism’s vertical position than its
proximity to the nodule summit. Therefore,
calculations of densities at distances from
the base (d) were made by dividing the nodule into concentric elliptical rings, each 0.5
cm wide. The areas of these rings (ad) were
calculated by approximating the nodule as
part of an ellipsoid subtended by an ellipse
with major and minor axes I 1 and I,:
ad = ~(1, - d + 0.5)(12 - d + 0.5)
-4u2-4
--a
where d is distance from nodule base, I 1 is
maximal diameter of nodule, and I2 is nodule diameter normal to I 1. This equation
simplifies to
ad = 0.5n(1, + I2 + 2d + 0.5). (6)
Since the nodules were irregular in outline, the area of the innermost ring was calculated by subtracting the outer rings from
the total nodule area. Organisms were assigned to the appropriate ring according to
their distances from the base.
For each taxon, the values for cover and
density were ranked in the concentric rings
on all nodules. A nonparametric Spearman
rank correlation coefficient (rS,with correction for ties; Siegel 1956) was calculated by
comparing the ranked values to their positions relative to the summit or base. For
example, in the summit analysis, a positive
r, indicates the taxon increases in density
1252
Mullineaux
(or cover) toward the summit. Taxa whose
densities (or cover) decrease away from the
summit have negative r, values and are more
appropriately analyzed with respect to their
proximities to the base. These two separate
analyses are not independent, but are differentially sensitive to summit-associated
and base-associated distributions on ellipsoidal or off-round nodules.
An r, value was calculated for each taxon
found on each of 34 nodules. Nodules had
been selected randomly from four box cores,
which were chosen to represent the range of
nodule sizes and nodule areal cover found
at the North Pacific field site. Individual rs
values for each of 46 taxa (those found on
two or more of the 34 nodules) were arcsinetransformed and pooled, and a two-tailed
t-test (Sokal and Rohlf 198 1) was used to
test for differences between the mean r, and
the value of zero expected if there were no
zonation. This somewhat indirect approach
was used for two reasons: nodules were not
all the same size, so direct comparisons of
ranked densities could not be made; and,
individual r, values could not be tested for
significance with any power because the
number of rings in each comparison was
small. Spearman correlation coefficients
were also calculated for distributions of suspension- and deposit-feeding groups. Direct
observations on feeding by deep-sea invertebrates are rare, so the feeding types of the
nodule epifaunal taxa were inferred. Deepsea metazoans were categorized as deposit
or suspension feeders according to the
known feeding habits of shallow-water congeners with similar morphologies. Foraminiferal taxa, whose feeding habits are
poorly known even in shallow water, were
categorized using their functional morphology. Those with upright or tubular test
structures were classified as suspension
feeders and those lacking upright structures,
or found under nodules or in subsurface sediment (as well as on the upper nodule surfaces), were grouped as deposit feeders.
These groupings of foraminifera1 taxa (listed
by Mullineaux 1987) are consistent with
available information on feeding of benthic
foraminifers (Christiansen 197 1; Sleigh
1973; DeLaca et al. 1980; Lipps 1983; Jones
and Charnock 1985). One deviation from
previous work is the classification here of
Saccorhiza ramosa as a deposit feeder. Individuals observed in this study occurred
on both upper and lower sides of nodules,
were attached to the nodule along the entirety of their tubes, and lacked the upright
feeding structures noted by Altenbach et al.
(1987).
Faunal distributions were also analyzed
with respect to nodule surface texture. Nodules tended to be rough at the base and
smooth near the summit, but they occasionally had patches of rough texture near
the summit or smooth patches near the base.
Surface areas of each texture were estimated
by recording the texture under each point
of a randomly arranged grid of points draped
over the nodule. The relative frequencies of
smooth and rough “points” in each ring of
the nodule were used to estimate the actual
areas covered by each texture. This procedure was unbiased (relative to the nodule
base and summit), but area estimates were
precise only to within 1O-l 5%. The abundances (and covers) of each taxon found on
the smooth portions of a ring were divided
by the fraction of the ring that was smooth
in order to calculate densities and percent
cover on the smooth portion. Individuals
found on rough texture were analyzed similarly. A one-sample, two-tailed t-test was
used for each taxon to find significant differences in density (or cover) between the
smooth and rough parts of 34 nodules. It
was also applied to the deposit- and suspension-feeding groups.
Results
Flow and particle accumulation -The
flume experiments showed that attached eddies form in the wakes of individual nodules
in an array under flow conditions similar to
those found at the North Pacific study site
(Table 1). An attachment point (where the
direction of flow along streamlines is toward
the nodule) formed on the upstream side of
the nodule (Fig. 1). A separation point (the
direction of flow along streamlines is away
from the nodule) formed on the downstream side of the nodule above a bilobed,
trapped eddy. This separation point moved
downstream from the nodule at slower flows.
The trapped eddy developed at all experi-
.
Epifaunal distributions on nodules
1253
:-=-yJif=-.Fig. 1. Oblique view of streamlines over a manganese nodule mimic. Diagram generalized from patterns of dye streams released over a nodule array with
46% areal cover at a shear velocity (u*) of 0.38 cm s-l;
measured over the 2.5-m-long nodule array. Locations
of the separation (S) and attachment (A) points vary
with U* and nodule cover, but the general shape of the
wake eddy is consistent over a range of u* = 0.23-0.69
cm s-l.
a
mental shear velocities, which cover much
of the range occurring at the abyssal field
site. Both the separation and attachment
points moved upward toward the nodule
summit as flume shear velocity increased
(Fig. 2).
Particle accumulation onto sticky nodules increased significantly (P < 0.05, oneway ANOVA) from the summit to the base
in all but the slowest experimental flows
(Fig. 3). Particle counts were normalized by
the ratio of total particle accumulation on
each nodule to mean particle accumulation
on three replicate nodules at each u*. Examination of the raw data, when compared
with the flow visualizations, showed that
enhanced deposition under the wake eddy
is responsible for the enhanced deposition
observed in the pooled samples from 0.5
and 1.Ocm above the base. In the slow flow,
accumulation at 1.0 cm above the base of
nodules was slightly higher than near the
summit (at 1.25 cm), but also slightly (and
significantly) higher than 0.5 cm above the
base. This anomalous decrease in particle
accumulation between 1.O and 0.5 cm is
relatively small (x4%) and is just as likely
to be due to changes in the trapping capacity
of the adhesive as to a decrease in contact
rates (see methods section). Although the
Heat Sink compound retains particles once
they adhere, fewer particles adhere to vertical than horizontal surfaces. The surface
of a nodule mimic becomes progressively
more vertical toward the base, and a small
decrease in measured accumulation toward
the base may be an artifact.
Shear
Velocity
(cm
s-’ )
Fig. 2. Height above bottom of upstream attachment (dashed line) and wake separation (solid line) as
a function of u*. Mean and standard deviation of three
measurements are plotted for nodule mimics 2.0 m
downstream from the leading edge of the 2.5-m-long
array.
Epifaunal distributions-Distributions
of
45 taxa (those occurring on two or more of
the 34 nodules) were documented for comparison with vertical position and nodule
surface texture. Individual taxa whose distributions were significantly correlated with
distance from the summit or base (two-tailed
t-test, P < 0.05, on Spearman correlation
coefficients) or whose abundance or cover
was significantly higher on one surface texture than the other (P < 0.05, two-tailed,
one-sample t-test) are listed in Fig. 4. Twelve
taxa ( 10 foraminifers, a xenophyophore, and
a serpulid polychaete) were most abundant
near the nodule summit, decreasing significantly in density or percent cover toward
the nodule base. Eleven taxa (nine foraminifcrs, a xenophyphore, and a tube-building
harpacticoid copepod) were most abundant
at the nodule base, decreasing in density or
cover toward the summit. Many of these 23
taxa were numerical dominants and 65% of
the total number of individuals belonged to
these vertically zoned taxa. Distributions of
many common taxa were also strongly correlated with surface texture, with 16 occurring predominantly on smooth surfaces and
nine occurring on rough surfaces. Over 68%
of the total individuals belonged to taxa correlated with surface texture.
1254
Mullineaux
Lszi
1.25
1.00
.50
--I
0
IO
0
IO
20
30
40
1.25
5
1.00
50
1
1.25
1 .oo
.
1
20
*
G--To
Although a significance level of P < 0.05
is appropriate for testing the distribution of
an individual taxon, the level should be adjusted for multiple testing. To yield an experiment-wise error rate (Sokal and Rohlf
1981) of 0.5 requires the cy level of each
comparison to be set at P < 0.00 1. Few taxa
are significant at this level (Fig. 4). Thus, to
avoid ignoring potentially interesting trends,
I consider distributions significant at the P
< 0.05 level in my discussion.
Many taxa were correlated with both texture and vertical position. Ten taxa occurred in higher abundance or cover near
the summit and on smooth surfaces, while
five taxa were found near the nodule base
and on rough surfaces (Fig. 4). The relative
effects of position and texture on the density
and cover of these taxa were investigated
by reanalyzing the data with multiple linear
regression. Only nodules of equal size (h 10
cm in diam) were used to make absolute
position (centimeters above the seafloor) and
relative position (proximity to the summit)
comparable between nodules. The rings were
grouped into two zones: summit (inner 3
cm) and base (outer 2 cm). Density and cover of individual taxa were calculated for the
areas covered by each of the two textures
(rough and smooth) in each of the two zones.
Partial regression coefficients (calculated
from log- transformed density and cover
values) for several of the less common taxa
were not significant in this reanalysis because the sample size was reduced from 34
to 11 nodules. Of the taxa that were significant, however, all had higher regression
coefficients for texture than position (Table
L/1_*6g
*
.50
2).
=
0
Particle
10
20
30
Accumulation
40
(mrrT2)
Fig. 3. Accumulation of suspended particles (~63
pm) onto sticky nodule mimics at three shear velocities
(u* in cm s-l). Particle density measured in eight, equally spaced, 0.64-mm* quadrats at three heights on the
nodule and pooled for each height. Plotted are mean
and standard deviation for pooled densities, normalized by ratio of total particle density on each nodule
to mean density on three replicate nodules at each u*.
Asterisks indicate heights with significantly enhanced
accumulation (one-way ANOVA with a posteriori Student-Newman-Keuls test, P < 0.05).
Nearly half (42) of the 86 taxa found on
the 34 nodules were classifiable as suspension feeders or deposit feeders. Many, however, were rare and few were among the
common taxa listed in Fig. 4. Of the 12
summit-associated taxa, only the serpulid
worm was taxonomically and morphologically close to shallow-water suspensionfeeding species; the other 11 taxa were protozoans that lacked upright tubes or other
upright test structures and are of unknown
feeding type. Four of the base-associated
taxa (Trochammina sp., Rhizammina aK.
algaeformis, Rheophax sp., and Hormosina
globulzfera -all agglutinated foraminifers)
1255
Epifaunal distributions on nodules
TEXTURE
POSITION
Base
‘2 Ammotrochoides
dark stercomere
mat
xenophyophore
sp.
‘s2 Plocopsilina
confusa
Is2 Pseudowebbinella
’ beige granular
mat
2 Tumidotubus
green chambered
mat
serpulid
polychaete
(S)
2 deflated
chambers
white crust
2 smooth
green mat
2 beige anastomosing
tunnels
Hemisphaerammina
marisalbi
tuft sponge
(S)
white granular
mot
2 tanaid,
Leptognathia
(D)
hydrozoan
sp. (S)
Tholosina
bulla
Saccorhiza
ramosa
(D)
2 Rhabdommina
neglecta
(S)
beige mat with filoments
beige mat
2 Rhizammina
off. algaeformis
thin cemented
tunnels
‘2 Hormosina
globulifera
(D)
t Rheophox
(0)
’ beige crust
xenophyophore,Semipsammina
’ harpacticoid
copepod
(D)
‘v2 large flexible
tubes
Trochammina
(D)
Cover
Density (cmb2)
Cover (rs 1
Rough
Summit
Smooth
Rough
(%I
Smooth
2
(D)
i
Fig. 4. Distribution of taxa (density in individuals cm-* and cover in percent) with respect to vertical position
on the nodule (position rJ and nodule surface texture (texture association). Mean Spearman rank correlation
coefficients (rs = O-l) are plotted for taxa whose abundances are significantly correlated with distance from the
nodule summit or the nodule base (one-sample, two-tailed t-test; y1= 34 or fewer nodules; P < 0.05 or IP <
0.001). Texture association is displayed as mean difference between density (or cover) of taxa on the smooth
and the rough surfaces of nodules (one-sample, two-tailed t-test; n = 34 or fewer nodules; P < 0.05 or zP <
0.001). Feeding type designated as suspension feeder (S) or deposit feeder (D) if known.
were also found occasionally on the nodule
undersides and in subsurface sediment and
are thus likely to be deposit feeders. The
harpacticoid copepod probably also deposit
feeds.
Rare taxa were included in the feeding
analyses by combining all the suspension
feeders into a suspension-feeding group and
all deposit feeders into a deposit-feeding
group. The distributions of these groups with
respect to the base and summit as well as
to surface texture were analyzed with the
Table 2. Partial regression coefficients from multiple linear regression on distributions (density and cover)
of taxa whose locations correlated significantly with both the nodule summit and smooth texture or with both
the nodule base and rough texture (Fig. 4). Equally sized nodules were necessary for this analysis, so sample
size was reduced to 11 nodules. Shown here are taxa with at least one significant correlation coefficient in the
1l-nodule sample (two-tailed; df = 44 or fewer). Asterisks: *-P -C 0.05; **-P < 0.01
Density
df
Texture
Cover
Position
Texture
Position
Summit and smooth
Ammotrochoides
Placopsilina confusa
Beige granular mat
Tumidotubus
Deflated chambers
Base and rough
Hormosina
globul$era
Large flexible tubes
44
44
44
44
44
0.57**
0.56**
0.47**
0.77**
0.60**
0.27*
0.19
0.28*
0.11
0.18
0.50**
0.34*
0.52**
0.43**
0.62**
0.49**
0.12
0.25
0.09
0.28*
42
42
0.33*
0.50**
0.08
0.43*
0.39*
0.53**
0.18
0.34
1256
Mullineaux
Table 3. Correlations of feeding-group distributions with position on nodule and nodule surface texture.
Correlation of feeding group distributions with respect to nodule summit and base tested with Spearman’s mean
rank correlation coefficient (r,). Correlation with texture tested by comparing feeding group abundance between
smooth and rough nodule surfaces. Taxa were grouped into suspension feeders, deposit feeders, and total
individuals. N is the number of nodules supporting each faunal group. Only positive r, values were tested against
zero (explanation in text).
Faunal
group
Suspension
Deposit
All taxa
Test
Summit r,
Base r,
Smooth
Rough
Summit r,
Base r,
Smooth
Rough
Summit rs
Base rs
* r, of suspension > r, of deposit; P < 0.05, two-samDIe,
two-tailed
t r, > 0; P < 0.05, one-sample,
two-tailed
f-test.
two-tailed
t-test.
$ Rough > smooth; P < 0.05, two-sample,
N
22
22
22
22
26
26
26
26
34
34
Mean density
(No. cm-*)
0.09(0.44)*
-0.08(0.46)
0.03(0.03)
0.03(0.06)
-0.28(0.29)
0.42(0.32)?
0.04(0.06)
0.24(0.19)$
0.50(0.37)j.
-0.57(0.33)
Mean cover (96)
0.06(0.42)*
0.02(0.44)
0.04(0.07)
0.03(0.04)
-0.34(0.22)
0.45(0.29)?
0.07(0.15)
0.85(1.41)$
0.42(0.44)-j-0.30(0.45)
t-test.
same techniques as the distributions of individual taxa (Table 3).
These feeding-group analyses showed that
although abundance of the suspension-feeding group tended to be high near the summit
and decreasetoward the base, this trend was
not significant at P -C 0.05. Abundance of
the suspension-feeding group was, however,
correlated more strongly (P < 0.05) with
proximity to the summit than was abundance of deposit feeders. This finding suggests that the center of distribution for suspension feeders was closer to the summit
than the center of distribution of deposit
feeders. Suspension-feeder abundances and
cover were not significantly different between rough and smooth surfaces. Depositfeeder abundances, however, were significantly correlated with both proximity to the
nodule base and rough surfaces. Multiple
regressions of feeding group distributions
against surface texture and position on nodules (with methods identical to those used
on individual taxa) produced no significant
correlations (possibly due to the reduced
sample size) and are not presented here.
The total density and cover of uncategorized (with respect to feeding type) taxa
increased significantly toward the nodule
summit. These taxa were numerically abundant, so the total number of individuals of
all taxa combined also increased toward the
summit. Many of the taxa responsible for
this trend in total density and cover are mat-
like, encrusting foraminifers of unknown
feeding types (illustrated in Mullineaux
1988a).
Discussion
A conspicuous feature of the structure of
epifaunal communities on manganese nodules is a vertical zonation of most dominant
taxa. Some of the taxa are strongly associated with smooth textures, which are usually at the nodule summit, and others with
rough textures, often found at the nodule
base. These correlations may be due to settlement responses of larvae and propagules
to texture. Other taxa have distributions
correlated with the vertical gradients in
boundary shear stress, horizontal particulate flux, and particle contact rates on nodule mimics demonstrated in the flume. These
patterns may be due to settlement responses
to flow or to postsettlement responses to
food availability. Since flow and surface texture both vary vertically on a nodule, it is
difficult in some casesto resolve their effects
on the fauna.
Flow similarity betweenjlume and$eldSimilarity between the flume flows and flows
at the deep-sea field site can be seen in a
comparison of shear velocities and bottom
roughnesses between the two environments
(Table 1). Preserving the field ratio of nodule height to boundary layer height (to
achieve strict scaling, sensu Southard et al.
1980) was not possible in a depth-limited
Epifaunal distributions on nodules
boundary layer in the flume. Full-scale
models of nodules were used in the flume
so that full-scale particles could be used for
the accumulation experiments. The nodules
protruded into only 12.5% of the flume water
depth, however, and did not distort the water
surface. The use of 2.5-m-long arrays of
nodules ensured that measurements at the
downstream end were taken in a fully developed boundary layer (without measurable downstream gradients, Paola 1985).
The effects of oscillating, omnidirectional
currents must be imagined in order to generalize flume observations to the deep seafloor. Although changes in current direction
are of sufficiently low frequency and nodule
fields are sufficiently large to model the currents as steady, unidirectional flows, currents oscillate on tidal and longer time scales
(Hayes 1979). Boundary shear patterns will
change orientation as current direction varies. Consequently, particle accumulation
patterns, which integrate over flow oscillations, should be radially distributed over the
whole nodule as the wake rotates with current direction. Thus, a gradient in accumulation of “sticky” particles such as larvae, increasing from the base to the summit,
is expected to occur. Enhanced deposition
of “nonsticky” food particles-a process that
depends on both particle contact and subsequent erosion - should also occur at the
nodule base since particle erosion is likely
to be greatest at the summit where flow accelerates over the nodules and decrease toward the base where the drag of the seafloor
slows the flow. Erosion is particularly low
under the wake, where shear stress is reduced (Paola 1983), and Brayshaw et al.
(1983) demonstrated wakes to be areas of
enhanced deposition. Further evidence for
this deposition zone on the nodule perimeter is provided by seafloor photos from the
central North Pacific showing nodules with
a thin flocculent layer of sediment covering
the periphery (R. R. Hessler unpubl. data).
Faunal distributions resulting from biological responses to flow are therefore expected to occur in radial patterns since mean
directionality in currents at the study site is
weak (Hayes 1979). To test this assumption,
I investigated directionality in faunal distributions in a preliminary analysis of fau-
1257
nal abundance in the 12 sectors of each nodule. No directional trends were found on
any of the nodules, and x2 tests were nonsignificant at P < 0.05 (although the power
of these tests was admittedly low).
Given the flume measurements discussed
in this section and the probable flow regimes
at the field site, some generalizations can be
made about particle flux past and onto nodules in deep-sea flows. Since flow accelerates
over the summit of nodules, horizontal particle flux is likely to be greater past the summit than past the nodule base in the absence
of a vertical particle concentration gradient.
In addition, boundary shear stress is likely
to be higher at the summit, due to flow acceleration and the absence of flow separation. Finally, particle contact is enhanced at
the nodule base and particle erosion is assumed to be reduced near the base, so in an
oscillatory flow both contact and deposition
are likely to be greater at the nodule base
than at the summit.
Settlement and feeding--In shallow-water
encrusting communities, distribution patterns of adults often reflect patterns of larval
settlement (Caffey 1985; Connell 1985;
Gaines and Roughgarden 1985). If postsettlement processes do not substantially alter
settlement patterns on hard substrates in
deep water, then distribution patterns of
adults on nodules may reflect contact rates
of larvae transported passively to nodule
surfaces. Several studies (seeButman 1987)
have suggested that larvae are carried passively in currents until they reach microhabitats where the flow velocities are sufficiently low that they can maneuver and
actively select a settlement site. Small, deepsea propagules, many of which are singly
flagellated cells, 5-50 pm in diameter, are
relatively poor swimmers (Grell 1967) and
might be expected to settle very near where
particles of similar settling velocities are deposited. If passive settlement occurs on
nodules and if settlement patterns persist in
adult distributions, then high densities of
organisms would be expected to occur near
depositional areas. Flume studies conducted in this and other studies suggest that net
particle contact and deposition should be
greater at the base than the summit of nodules in the field. A corresponding distribu-
1258
Mullineaux
tion of adults was not found; instead the
total number of individuals increased toward the summit. The observed distributions indicate that most of the epifaunal organisms are either not settling passively on
the spatial scale of an individual nodule or
their settlement patterns do not persist.
An alternative explanation for flow-related distributions is active settlement responsesto flow. Crisp (195 5) found that barnacle larvae actively avoided settling onto
substrates under low shear. Under very high
shear, however, the larvae were unable to
attach, so they settled only under an intermediate range of shear stresses. If deep-sea
larvae exhibit comparable active responses
to shear, then those with preferences for low
shear stress might settle near the base of a
manganese nodule, while those preferring
higher shear stress might settle closer to the
summit. If these settlement patterns persist,
then a vertical stratification in the faunal
distributions would result. Most individuals (> 65%) living on manganese nodules
belonged to taxa whose abundances were
significantly correlated with vertical position on the nodules. Many of the remaining
taxa which did not show vertical distributions were rare and may have had nonsignificant correlations because of small sample size. Thus, the hypothesis that settlement
responses to shear account, for much of the
pattern observed on nodules cannot be rejected. Although many ofthese 23-taxa were
also correlated with surface texture (some
even more strongly than with vertical position, Table 2), a stronger response to shear
was demonstrated for eight of the vertically
zoned taxa.
Active settlement responses to texture can
also explain some of the faunal distributions
observed on manganese nodules. Larvae are
known to settle in response to different surface textures in shallow water (e.g. Barnes
1956; Crisp and Barnes 1954). The hypothesis that deep-sea propagules can maneuver
well enough to settle actively in response to
surface texture is supported by the distribution patterns of at least 22 taxa on the
nodules. Fifteen taxa were relatively more
abundant on smooth surfacesand seven were
more abundant on rough surfaces (Fig. 4).
Eight of these 22 taxa were correlated in
abundance with texture only (independent
of position on the nodule). A multiple
regression analysis suggested that abundances of at least seven of the remaining 14
taxa are more strongly correlated with texture than with position (Table 2).
The use of observed adult distributions
to address questions about settlement rests
on the assumption that postsettlement
events have not substantially altered settlement patterns. Adult food requirements may
be important in structuring communities on
nodules, however, and food availability may
alter initial settlement patterns.
In general, deposit feeders are found in
low-shear, depositional
environments
(Sanders 1958; Hessler and Jumars 1974;
Hughes 1975). In the present study, deposit
feeders were expected to dominate in zones
of relatively slower current and higher deposition on the manganese nodules. Flume
studies showed that accumulation is enhanced at the base of a sticky nodule, indicating that deposition would also be greater along the base due to the absence of
accelerations found over the summit and to
the relatively low shear stresses under the
wake. A decrease in abundance (and cover)
of the combined deposit-feeding group from
the nodule base to the nodule summit is
consistent with this hypothesis. Distributions of individual deposit-feeding taxa,
when analyzed taxon by taxon, also support
the hypothesis. Five deposit feeders (Trochammina sp., Rhizammina aff. algaeformis, Rheophax sp., Hormosina globulifera,
and the tubicolous harpacticoid copepod)
increased in abundance toward the base, but
none increased toward the summit.
The combined deposit-feeding group,
however, is strongly correlated with rough
surfaces as well as with flow patterns. Since
a rough surface may be more likely to retain
food particles than a smooth one, an alternate hypothesis is that surface texture causes enhanced food deposition and, ultimately, high abundances of deposit feeders near
the base. These two hypotheses need not be
mutually exclusive, and enhanced deposition at nodule bases is likely to be due to a
combination of high particle contact rates,
Epifaunal distributions on nodules
low shear stresses, and rough surface textures.
Suspension feeders are often found in
areas of high particulate flux (Ebling et al.
1948; Pequegnat 1964; Riedl 197 1; Hughes
1975; Genin et al. 1986). Taxa with this
feeding habit were expected to dominate in
zones of relatively higher current over manganese nodules. The suspension-feeding
group was found farther from the nodule
base than deposit feeders, which is consistent with the premise that suspension feeders occur in areas of higher mean flow velocities than deposit feeders. The suspension
feeders as a group, however, did not dominate the nodule summit, which was presumed to be the region of greatest horizontal
particulate flux. Instead, their abundances
had a center of distribution midway up the
nodule.
This unexpected midnodule peak in
abundance of suspension feeders could be
due to one of several factors. If the concentration of suspended particles decreasesfrom
the seafloor to the height of nodule summits, then their maximal horizontal fluxes
might occur below the summit. Vertical gradients of suspended particles on spatial scales
of a few centimeters above the seafloor
would not be expected for relatively small
particles or strong flows (Rouse’s diffusional
theories, Yalin 1972). The calculations for
a midrange flow in the deep sea (u* = 0.3
cm s-l), however, suggest that silt-size particles with fall velocities of 0.05 cm s-l would
be almost twice as concentrated at the nodule summits (1.5 cm) than near the bases
(0.5 cm). Thus, a substantial concentration
gradient in some food particles may occur
occasionally in slower flows at the study site.
An alternate explanation for low suspension-feeder abundances at nodule summits
is that the environment there (e.g. the higher
shear stress) does not promote recruitment
of their larvae, even though it is the optimal
location for adult feeding. In this case, suspension feeders would increase in abundance as food availability increases, up to
an intermediate height, but be scarce at the
summit where the larvae are unable to recruit.
Community structure on nodules-The
1259
vertical stratification of epifaunal taxa on
nodules is consistent with patterns expected
from adult feeding preferences in flow and
from active larval responses to surface texture or boundary shear stress. The distribution patterns of most taxa are not consistent with the hypothesis that adults persist
on the areas where the supply (contact) of
their larvae is greatest. Several questions,
however, have been left unresolved since
vertical distributions of some individual
taxa could be due to either surface texture
or flow. In addition, alternate hypotheses,
such as competition for space or predation,
cannot be ruled out.
One possible reason that effects of texture
and flow are so difficult to resolve in this
habitat is that they interact. Vertical relief
of the botryoids is small relative to the
thickness of the viscous sublayer over the
nodule surface and probably does not alter
the overlying velocity profile. Nevertheless,
a rough surface may provide larvae with
better attachment sites and allow them to
settle under a greater range of shear stresses
than a smooth surface. In addition, in a given flow, deposition onto a rough surface may
be enhanced over a smooth one, since particles could be retained in depressions. Finally, surface texture and particle accumulation patterns on a nodule may, in some
cases, be causally related. Dymond et al.
(1984) suggestedthat the rough surface area
forms during diagenetic accretion while the
nodule surface is in contact with sediment.
This process usually occurs only on the underside of the nodule, but nodules often have
a flocculent layer of sediment covering the
peripheral edge. In this case, the depositional environment would be controlling the
nodule surface texture and their relative effects would be indistinguishable.
The use of flow patterns over nodules to
predict, a priori, the distribution patterns of
epifaunal organisms is a means of determining the relative importance of biological
vs. physical processes in structuring deepsea communities. If observed patterns are
consistent with predictions from hydrodynamic studies, then flow mediation cannot
be ignored as a contributing factor. This information can then be used to design in situ
1260
Mullineaux
experiments to distinguish between the remaining alternative hypotheses. One such
experimental study (Mullineaux 1988b) was
conducted in deep water to examine the response of hard-substrate larvae to nodules
of varying textures under varying flow regimes. After a 7-week deployment, no difference was found between recruitment onto
smooth and rough nodules, but a significant
difference was found between nodules raised
20 cm above the seafloor and those resting
on it. After 2 yr, there was still no colonization response to texture, but suspension
feeders dominated the raised nodules and
deposit feeders dominated the lower ones.
These results suggestthat benthic organisms
exhibit both settlement and postsettlement
responses to flow, but no detectable response to texture. This experimental study
provides further support for the suggestion
that texture-related faunal distributions observed in the present study result from interactions between texture, flow, and particulate food availability, rather than texture
alone.
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Submitted: I I April I988
Accepted: 28 June 1989
Revised: 1I August X989