Coral Reefs (2006)
DOI 10.1007/s00338-006-0089-6
R EP O RT
Tara Oak Æ Robert E. Scheibling
Tidal activity pattern and feeding behaviour of the ophiuroid Ophiocoma
scolopendrina on a Kenyan reef flat
Received: 19 June 2004 / Accepted: 16 December 2005
Springer-Verlag 2006
Abstract Ophiocoma scolopendrina exhibits a distinctive
pattern of feeding activity on intertidal reef platforms off
Kenya. With the first wave of the flooding tide, dense
aggregations of these ophiuroids (up to 320 m 2) engage
in a 1–2 min burst of surface-film feeding, vigorously
sweeping the air-water interface and associated sea foam
with the ventral surface of 2–4 arms. Suspension feeding
(with arms extended in the water column) is the primary
feeding mode throughout the rest of the tidal cycle
(involving 25–65% of the population at a time), while
bottom feeding (with arms extended along the substratum) is infrequent (<10%). Field experiments showed
that surface-film feeding is regulated by water depth and
can be triggered by suspended particles. This feeding
mode appears to be an adaptation to the intertidal
habitat, enabling the ophiuroids to exploit a nutrientrich surface film during a temporal refuge (low tide)
from fish predation. Dense populations of O. scolopendrina may represent an important trophic link between producers of particulate organic material and
higher-level consumers in coral reef environments.
Keywords Æ Feeding behaviour Æ Intertidal zone Æ
Ophiocoma scolopendrina Æ Ophiuroid
Introduction
Ophiuroids exhibit a variety of feeding mechanisms but
generally separate into two main feeding types based on
prey size: (1) species which consume large prey
Communicated by Environment Editor B.G. Hatcher
Tara Oak and Robert E. Scheibling contributed equally to this
paper. The order of authorship is alphabetical
T. Oak Æ R. E. Scheibling (&)
Dalhousie University, B3J 4H1, Halifax, NS, Canada
E-mail: rescheib@dal.ca
Tel.: +1-902-4942296
Fax: +1-902-4943736
(carnivores and scavengers), and (2) microphagous
feeders which extract plant animal and detrital particles
from the water column or substratum (suspension and
deposit feeders) (Warner 1982; Lawrence 1987). Different behavioural and morphological adaptations characterize the primary feeding modes, although some
species are generalists using alternative prey capture
mechanisms. The success of ophiuroids in the benthic
marine environment has been attributed to this diversity
of feeding habits (Fontaine 1965). Ophiuroids are highly
vulnerable to predators and most shallow-water species
are cryptic and expose only their arms to capture food
(Aronson 1991; Munday 1993; Bourgoin and Guillou
1994). Where the threat of predation is low, some species
emerge from refuges to feed although increased conspicuousness may have severe costs in terms of survival
(Aronson and Harms 1985).
The genus Ophiocoma has a circumglobal distribution
in the tropics and subtropics with the greatest number of
species in the Indo-Pacific (Devaney 1974). Species of
this genus are among the most abundant ophiuroids in
intertidal and shallow subtidal reef habitats around
atolls, islands and continental margins. They are primarily microphagous feeders and employ a variety of
suspension and deposit feeding mechanisms (Chartock
1983). One species, Ophiocoma scolopendrina (Lamarck),
which inhabits intertidal reef flats, has evolved a specialized method of capturing neuston and detrital particles and films suspended at the air-water interface (Ely
1942; Magnus 1962; Chartock 1983).
On the flooding tide, O. scolopendrina emerges from
crevices and concealing vegetation to extend the ventral
side of its arms along the air-water interface and vigorously sweep this surface. Suspended particles and scum
are trapped on small mucous-covered spines that are
cleaned by the tube feet and transported as a bolus to the
mouth (Magnus 1962; Chartock 1983). At other stages
of the tidal cycle, O. scolopendrina engages in microphagous suspension- and deposit-feeding typical of
other members of the genus (Chartock 1983) and
ophiuroids generally (e.g. Pentreath 1970; Warner and
Woodley 1975; Loo et al. 1996). The disc remains hidden
in crevices or under vegetation and the arms are projected into the water column or along the substratum to
accumulate particles on mucous nets or mucous-covered
spines (Chartock 1983).
Our study, on an intertidal reef flat in Kenya, is the
first to quantify patterns of feeding activity and behaviour of O. scolopendrina in relation to the tidal cycle, and
to experimentally investigate factors associated with the
flooding tide (including depth, water flow, and suspended particulate material) that may trigger or regulate
surface-film feeding. We relate this unusual feeding
behaviour to tidal patterns in the availability of different
particulate food resources and the risk of predation. We
also examine the potential role of these ophiuiroids as a
trophic link between producers of particulate organic
Fig. 1 a The intertidal reef flat
at Tiwi Beach, Kenya, spanning
300 m from the shore (lower
right) to the seaward edge
where waves are breaking. The
arrow indicates a band of sea
foam delivered with the
flooding tide. Distant figures of
the researchers (in Stratum 5,
Table 2) are evident between
the band of foam (above the
arrow) and the edge of the reef
platform. Dark patches in the
foreground are seagrass. b
Ophiocoma scolopendrina
engaged in surface-film feeding
(SFF) with arms upturned and
sweeping the surface foam (two
individuals are indicated with
paired arrows on right). Also
shown is an individual that has
just completed surface-film
feeding and remains largely
exposed on the bottom (single
arrow on left); other individuals
have retreated to crevices with
just their arms exposed. The
band of foam is progressing
from left to right. c An
individual sweeping sea foam
with 3 arms during first contact
with the flooding tidal front. d
As water level rises the arms are
extended further to maintain
contact with the surface. e
Individuals with only the arm
tips in contact with the surface
during the last instant of
surface-film feeding. f
Individuals ascending seagrass
to retain contact with the
surface for feeding
material in coral reef environments and higher-level
consumers such as fish.
Materials and methods
Study site
Our study was conducted in March and April 2000 on
an intertidal reef flat at Tiwi Beach, Kenya (414’S,
3934’E). The reef flat (Fig 1a) extends 300 m across a
shallow gradient (<1% slope) from the high tide mark
to the seaward margin, where depth increases abruptly
to 3–4 m (below chart datum). Ophiocoma scolopendrina
was abundant on the reef flat between about 50 and
250 m offshore.
The substratum of the reef platform is porous limestone of Pleistocene origin (Ngusaru 1997) with overlying patches of sand, and turfs of seagrass (Cymodocea
rotundata) and macroalgae (mainly Cystoseira myrica,
Turbinaria decurrens, Padina boryana, and Laurencia
papillosa). Live corals are generally restricted to large
rifts in the platform along the outer edge and to the
deeper water beyond. Water depth, measured with a
graduated pole at fixed locations in each sampling
stratum (see below), ranged from 0 to 1.4 m at spring
tides, and from 0.1 to 0.5 m at neap tides. Shallow tide
pools (usually <20 cm deep) of varying dimensions
occur throughout the study area. Water temperature,
recorded at 5 min intervals by data-logging thermometers anchored on the reef flat at 170 and 60 m offshore
(Hobotemp Tidbits, Onset Computer Corp. Pocasset,
Mass, USA), ranged from 26 to 38C over the tidal cycle, occasionally reaching peaks of 40C in shallow pools
(measured by hand-held mercury thermometer) during
mid-day low tides.
Density and size structure
The density and size structure of Ophiocoma scolopendrina at Tiwi Beach was estimated by stratified random
sampling of the reef platform. Ophiuroids were counted
and measured in 20·20 cm (400 cm2) quadrats (n=25–
31) haphazardly placed along each of five belt transects
(2 m wide) extending 50 m in an alongshore direction
and spaced at 30 m intervals between 75 m and 195 m
offshore (Stratum 1–5). Data were pooled across strata
to describe the population. Disc diameter of ophiuroids
was measured in 3 mm size classes by matching the disc
against a template of seven squares increasing in
dimension by 3 mm increments from 3 to 21 mm. In
some cases (<10%), individuals could not be extracted
without damage from refuges in the substratum and
were counted but not measured. The length of the longest (non-regenerating) arm and disc diameter were
measured (1 mm accuracy with vernier calipers) in an
additional sample of 116 individuals to determine the
relationship between these metrics by linear regression.
These ophiuroids were narcotized in an isotonic solution
of magnesium chloride at a concentration of 72 gl 1 to
facilitate measurement and prevent arm loss.
Table 1 Classification of degree of exposure and feeding mode of
Ophiocoma scolopendrina
Exposure level
Low
Medium
High
Disc hidden in a crevice or hole,
at least 1 arm visible
Partly covered by vegetation,
disc and some arms visible
Disc and most or all arms fully exposed
Feeding mode
Surface-film
Suspension
Deposit
Arms sweeping the air-water interface
Arms suspended in the water column
Arms sweeping the substratum
roids were pooled over the ten quadrats to give sample
sizes ranging from 33 to 118 individuals (mean=82) per
sampling interval per day. The percentage of individuals
in each exposure level, and engaged in each type of
feeding, was calculated for each pooled sample. The
samples were then grouped in 2 h periods according to
tidal stage and averaged across sampling days. Depth at
fixed reference points (in Stratum 3) was recorded at the
beginning and end of each sampling interval.
The pattern of surface-film feeding was quantified in
greater detail by increasing the sampling frequency
during the first ‘‘wave’’ of incoming tide on four days.
This wave is a shallow tidal front that forms once the
rising sea begins to flood the platform. The front advances slowly (a few centimetres per second) towards
shore, generally carrying with it a conspicuous layer of
sea foam (Fig. 1a). On each sampling day, ten quadrats
of 400 cm2 were placed in areas of high ophiuroid density (6–22 individuals per quadrat). The proportion of
individuals engaged in surface-film feeding and the water
depth were recorded in each quadrat at approximately
12 min before, during, and 12 min after the first wave of
the incoming tide. Data from each sampling interval
were pooled over the ten quadrats on each day and
averaged across sampling days.
The number of arms used in surface-film feeding was
recorded by haphazardly sampling individuals at water
depths of 2–4 cm as the incoming tidal front progressed
over the platform. Data were pooled for samples taken
on three sampling days giving a sample size of 414
individuals.
Analysis of particulate food sources
Feeding behaviour and exposure
Patterns of exposure and feeding behaviour of Ophiocoma scolopendrina in Stratum 3 (120–150 m offshore)
were quantified by sampling ophiuroids at 1–2 h intervals throughout the daytime tidal cycle over five days.
For each sample, all visible ophiuroids within ten haphazardly-placed quadrats of 400 cm2 were classified
according to three levels of exposure (low, medium,
high) and three feeding modes (surface-film feeding,
suspension feeding, deposit feeding) (Table 1). Ophiu-
To compare the organic content of different particulate
food sources available to O. scolopendrina, surface sediment, seawater, and sea foam were haphazardly sampled at daytime low tides within an area of 10 m2 in
Stratum 1 (60–90 m offshore) over 3–5 days. Sediment
was collected by scooping the top 3 mm of fine sand into
a small plastic vial (3–13 g dry weight per sample).
Seawater from shallow tide pools was collected in 60 ml
syringes (0.4–1.8 l per sample) and filtered on glass-fibre
(GF/C) filters. Foam was collected with an aquarium dip
net and deposited onto glass-fibre filters (0.04–1.0 g dry
weight of particulate residue per sample). The samples
were dried and weighed, combusted in a muffle furnace
at 500C for 4 h, and then re-weighed to calculate ashfree dry weight and percentage of dry weight that is
organic matter. Replicate samples on each day (n=4–6)
were averaged for each particulate food source and
grand means were calculated based on daily averages.
trial. A paired samples t test was conducted, based on
these averages for each trial, to compare the depth and
time (from the start of the experiment) at which surfacefilm feeding peaked and ended between enclosed and
open treatments.
Field experiments
To examine the effect of suspended particles in triggering
surface-film feeding, experiments were conducted with
three particulate materials: fine sand from the surrounding area, carmine particles, and sea foam collected
near shore that was laden with organic material (giving
it a brownish tinge). Enclosed arenas (with solid walls)
were placed on the substrate at low tide approximately
30–60 min prior to the first wave of the flooding tide.
The arenas were placed in the same general area as
Experiment 1 but where there was sufficient water depth
for surface-film feeding. Three arenas were used in each
of three or four (for sea foam) trials: two were haphazardly selected to receive the experimental treatment and
the third was used as a control. The total number of
individuals and the number of individuals engaged in
surface-film feeding in each arena was recorded before
each trial.
The experimental treatment consisted of sprinkling
approximately 3 ml of sea foam with associated particulate material, 100 mg of dry sand, or 20–30 mg of
carmine particles onto the water surface enclosed by
each experimental arena. These amounts were sufficient
to disperse each of these particulate materials across the
water surface within an arena. The maximum number of
ophiuroids that were surface-film feeding during a 3 min
interval after the introduction of particulate substances
was recorded. The control treatment involved sprinkling
seawater over the arena.
Replicate treatment or control arenas were pooled
across experimental trials (which were conducted within
a 30 min period on the same day) for each type of particulate material. The percentage of individuals that
were surface-film feeding was compared between control
and experimental treatments by t test, and among
experimental treatments by 1-way analysis of variance.
Experiment 1
To examine environmental factors that may potentially
regulate surface-film feeding in O. scolopendrina, naturally occurring individuals were enclosed in cylindrical
plastic arenas (25 cm diameter, 10 cm height, 490 cm2 of
enclosed surface area) placed on flat sand and seagrass
substrata in Stratum 2 (90–120 m offshore). The effect of
the presence of sea foam, water flow and depth on
feeding behaviour was examined by comparing O. scolopendrina in enclosed arenas to open-sided control arenas. Control arenas had solid 3 and 2 cm-high rims
around the top and bottom, respectively, and three equal
panels cut out of the sides, separated by three evenlyspaced 5 cm wide supporting walls such that 81% of the
circumference between the two rims was open. They
presented some of the potential artefacts of the fully
enclosed (with solid sides) arenas, such as disturbance to
enclosed ophiuroids and sediments during deployment.
The base of each arena was driven 2–3 cm into the
sediment. This temporarily sealed off enclosed arenas
from the incoming tide while allowing water and foam to
flow naturally through the open sides of control arenas.
To test their efficacy as enclosures, a fluorescent red dye
(Rhodamine B, Sigma Chemicals) was released around
the outside perimeter of enclosed arenas immediately
after deployment.
Five arenas were used in each of six experimental
trials: three enclosed and two open arenas were positioned in random order perpendicular to the direction of
the incoming tide with 2 m spacing between arenas.
The arenas were placed in areas with <2 cm of overlying water and relatively high ophiuroid density 5–10 min
before the incoming tidal front washed over the area.
Within 1 min after deployment, initial water depth, the
total number of individuals (7–21 per arena), and the
number that were surface-film feeding were recorded in
each arena. Depth and the number of individuals surface-film feeding were then recorded at 20–60 s intervals
as the front passed over the area, until all surface-film
feeding ceased in the arenas. Replicates were discarded
(no more than one per treatment per trial) if seepage
around the base occurred in enclosed arenas or if water
levels rose too rapidly in open-sided controls to attain a
reliable count of feeding individuals. The percentage of
individuals surface-film feeding at each sampling interval was calculated and averaged across two or three
replicate arenas for each treatment in each experimental
Experiment 2
Results
Density and size structure
Mean density of O. scolopendrina ranged from 7.9 to
12.8 individuals per 400 cm2 among strata on the
intertidal platform at Tiwi Beach (Table 2). The mean
density pooled across all strata was 9.9 individuals per
400 cm2 (or 248 individuals m 2). The size-frequency
distribution (as disc diameter) was similar among strata,
and approximately normal about a modal class of 9 mm
and class range of 3–18 mm for individuals pooled
across all strata (n=1265) (Fig. 2). The 3 mm size class
Table 2 Density of Ophiocoma scolopendrina (individuals/400 cm2)
in transects sampled at 30 m intervals offshore within each of five
strata on the reef flat at Tiwi Beach, Kenya
Stratum
Distance offshore (m)
Density (/400 cm2)
n
1
2
3
4
5
75
105
135
165
195
12.8±5.6
10.0±5.9
7.9±4.0
10.3±4.0
8.5±4.3
27
30
29
31
25
Data are mean ± SD for n quadrats in each stratum
may have been under-sampled because small ophiuroids
were particularly cryptic and difficult to collect for
measurement. Regression analysis, based on a sample of
116 ophiuroids ranging from 4 to 18 mm in disc diameter, showed a strong linear relationship (r2=0.978)
between of arm length (L) and disc diameter (D):
L=4.816D. Thus the modal disc diameter (9 mm) gives
a predicted arm length of 43 mm and the upper disc
diameter class of 15 mm (excluding larger individuals
which accounted for <1% of the population) gives a
predicted maximum arm length of 72 mm.
Feeding behaviour and exposure
The degree of exposure of Ophiocoma scolopendrina
varied with tidal stage (Fig. 3a). Ophiuroids were most
cryptic at or shortly before high tide, when 85–95% of
the population was hiding in crevices or holes in the reef
(Level 1, low exposure), and most exposed at low tide,
when 32% was covered only by vegetation and 11% was
fully exposed (Levels 2 and 3, medium and high exposure, respectively). Suspension feeding was the primary
feeding mode across all 2 h tidal intervals (grand
mean ± SD, 44±14%), with the highest frequency of
this feeding mode (65%) occurring shortly after high
tide (Fig. 3b). The frequency of bottom feeding was low
(<10%) throughout the tidal cycle, with a minimum
(1.4%) occurring around high tide. Surface-film feeding
could occur only at low tide, when water depth was only
a few centimetres.
Frequent sampling around the incoming tide indicated a burst of surface-film feeding in O. scolopendrina
as the tidal front washed over the platform (Fig. 1b),
with a mean of 47% of the population engaged in this
mode of feeding (Fig. 4). The ophiuroids rapidly vacated
their refuges to vigorously wave their arms along the airwater interface in an irregular pattern. Most used three
arms (67%, n=414) for surface-film feeding, and less
often two (15%) or four arms (13%) (Fig. 5). While
sweeping the water surface, they remained anchored to
the substratum or vegetation with at least one arm, often
turning the disc and arms entirely upside-down (Fig. 1c,
d). The ophiuroids usually were fully exposed in this
position. The activity lasted only a few minutes; the
frequency of surface-film feeding declined to <2%
within 12 min of the passage of the tidal front. As water
depth increased, contact with the surface decreased until
only the very tips of the arms remained (Fig. 1e). Some
ophiuroids prolonged the feeding period by ascending
vegetation (Fig. 1f). Once contact was lost, they lowered
their arms and retreated into refuges on the bottom.
Thus, as the tidal front progressed along the reef platform it was tracked by a translating wave of ophiuroid
arms, moving like a stadium full of exuberant armwaving fans at sporting event.
Particulate food sources
The suspended particles in the seawater over the reef flat
consisted of 74.7±8.2% organic matter by dry weight
(mean ± SD, n=4), however these were extremely dilute at only 22.8±6.3 mgl 1. The surface sediment
consisted of 5.3±1.4% (n=17) organic matter, and
particles in sea foam delivered by the incoming tide were
43.4±20.0% (n=32) organic matter.
Field experiments
50
Experiment 1
Frequency (%)
40
30
20
10
0
3
6
9
12
15
18
Disc diameter (mm)
Fig. 2 Disc diameter class frequency (%) of Ophiocoma scolopendrina on the reef flat at Tiwi Beach, Kenya (n=1265)
In open-sided control arenas, surface-film feeding generally peaked immediately upon exposure to the first
wave of the incoming tide and then dropped off quickly
as water depth increased. The solid walls of enclosed
arenas slowed the rise in water level within the arenas, as
water seeped in through the porous substrate. Depth in
enclosed arenas was consistently shallower, at any given
time, than in the control arenas and surrounding environment (Fig. 6). Therefore surface-film feeding in enclosed arenas peaked later and was sustained longer
than in open control arenas.
There was no significant difference between the enclosed and open arenas in the mean depth at which
a) Exposure Level
100
80
Low
Medium
High
Depth
90
80
70
60
70
60
50
50
40
40
30
30
20
20
10
10
0
0
b) Feeding Type
100
80
Suspension
Surface-film
Deposit
Depth
90
80
70
Depth (cm)
Frequency (%)
Fig. 3 Mean (+SD) frequency
(%) of Ophiocoma
scolopendrina in a three
exposure levels (low, medium
and high; Table 1), and b three
feeding modes (suspension,
surface-film, and deposit
feeding; Table 1) at 2 h tidal
stages on the reef flat at Tiwi
Beach, Kenya. Values at the
low tide interval are repeated
for graphical clarity. Mean
water depth at each tidal stage
is also shown
70
60
60
50
50
40
40
30
30
20
20
10
10
0
0
low
high
low
Tidal stage
surface-film feeding peaked or ended (Fig. 7a), although
the timing of these events differed significantly between
the treatments (peak: t5=3.723, P=0.007; end: t5=3.62,
P=0.008) (Fig. 7b). The peak in frequency of surfacefilm feeding occurred at a mean depth (averaged across
10
Feeding
Depth
8
60
6
40
4
20
2
0
0
Before
During
After
Tidal front
80
70
Frequency (%))
80
Experiment 2
Surface-film feeding was triggered by addition to arenas
of each of three types of particulate materials: sand, inert
(carmine) particles, and organic material associated with
Depth (cm)
Frequency (%)
100
both treatments) of 2.3±0.4 cm (mean ± SD); most
feeding had ended at a mean depth of 4.0±0.5 cm.
60
50
40
30
20
10
0
1
Fig. 4 Mean (+SD) frequency (%) of Ophiocoma scolopendrina
engaged in surface-film feeding about 12 min before, during, and
12 min after passage of the flooding tidal front on the reef flat at
Tiwi Beach, Kenya. Mean water depth at each tidal stage is also
shown
2
3
Number of arms
4
5
Fig. 5 Frequency (%) of the number of arms per individual of
Ophiocoma scolopendrina used in surface-film feeding on the reef
flat at Tiwi Beach, Kenya (n=414)
Fig. 6 Mean (+SD) frequency
of Ophiocoma scolopendrina
engaged in surface-film feeding
over time (since contact with
the first wave of the flooding
tide) in open (control) and
enclosed arenas during two
representative experimental
trials on the reef flat at Tiwi
Beach, Kenya
a) Trial 1
100
7
Enclosed feeding
Open feeding
Enclosed depth
Open depth
80
6
5
60
4
40
3
1
0
0
0
60
120 180 240 300 360 420 480 540 600 660
b) Trial 2
100
7
Depth (cm)
Frequency (%)
2
20
6
80
5
60
4
40
3
2
20
1
0
0
0
20
40
60
80
100
120
140
160
Time (s)
the surface foam. Less than 2% of ophiuroids in
experimental arenas were engaged in surface-film feeding before the addition of these materials. There was a
significant increase in the percentage of individuals engaged in surface-film feeding in treatment arenas (40–
a)
Mean depth (cm)
5
Enclosed
Open
4
3
70
SW Control
2
Added Particles
60
1
Frequency (%))
0
b)
350
300
Time (sec)
60%) relative to the respective sea water controls
(<5%) for each material tested (t test, P<0.001)
(Fig. 8). The percentage of individuals that was surfacefilm feeding was significantly higher for the treatment
with carmine particles than that with foam (F1, 12=4.1,
P=0.015). There were no significant differences between
carmine and sand, or sand and foam treatments.
The carmine particles and dry sand were of similar
consistency. Both formed a fine film of suspended
250
50
40
30
20
200
150
10
100
0
50
0
Sand
Carmine
Foam
Added Particle Treatment
Peak
End
Fig. 7 Mean (+SD) a depth and b time (since contact with the first
wave of the flooding tide) at the peak and the end of surface-film
feeding by Ophiocoma scolopendrina in open (control) and enclosed
arenas on the reef flat at Tiwi Beach, Kenya
Fig. 8 Mean (+SD) frequency (%) of Ophiocoma scolopendrina
engaged in surface-film feeding in arenas where particulate
materials (sand, carmine particles, sea foam) were added, and in
controls where only seawater was added, on the reef flat at Tiwi
Beach, Kenya
particles on the water surface and dispersed evenly
throughout the arena as they sank. Individuals
throughout an arena responded similarly, sensing the
sand or carmine particles with one or more arms, then
coming fully out of hiding to feed. The collected particles were clearly evident in the ambulacral grooves as
they were moved by tube feet from arm tip to mouth.
The foam used for this experiment was collected near
the shoreline. It was considerably denser than the foam
associated with the tidal front as it flooded the reef flat,
and contained stringy agglutinations of organic material. The particles in the foam usually sank quickly to the
bottom and did not distribute evenly within the arenas.
Within seconds, individuals in an arena congregated
where aggregates or strands of particulate material were
precipitating from the overlying foam. These strands or
clumps usually were grasped with one or more arms and
delivered to the mouth by a curling action of the arms.
Discussion
Ophiocoma scolopendrina inhabits the upper intertidal
zone on limestone reef platforms throughout the tropical
Indo-Pacific region and the Red Sea (Ely 1942; Devaney
1974; Clark 1976; Chartock 1983). It is the most abundant ophiuroid in this zone, where it usually occupies
small crevices in reef conglomerate or coral rubble. The
average density of O. scolopendrina in our study
(247 individuals m 2 across the reef flat and up to
320 individuals m 2 in one region) was higher than that
previously recorded in other areas. Devaney (1974) reported that this species occurs in aggregations of up to
50 individuals m 2 in Southeastern Polynesia. At
Enewetak, Marshall Islands, Chartock (1983) recorded a
maximum density of 100 individuals m 2, but densities
of 20 individuals m 2 were more typical. James and
Pearse (1969) noted that O. scolopendrina was the most
conspicuous intertidal ophiuroid on the Egyptian coast
of the Red Sea, but did not provide measures of abundance. The size range of O. scolopendrina at Tiwi Beach
(from about 3–18 mm disc diameter) was similar to that
recorded by Law (1995) in Fiji (1–22 mm) and Devaney
(1974) in Polynesia (up to 25 mm).
Among the Ophiuroidea, surface-film feeding as an
alternative microphagous feeding mechanism has been
reported only in O. scolopendrina. This mode of feeding
among intertidal ophiuroids can occur only at low tide
when the air-water interface is within arms’ reach. The
phenomenon also has been observed in Ophiocomina
nigra, but only in aquaria (Fontaine 1965). Because
O. nigra is predominantly a subtidal species, this unusual
feeding mechanism may be less important to its nutrition
than it is to O. scolopendrina, a strictly intertidal species
(Fontaine 1965).
Our observations of microphagous feeding behaviour in O. scolopendrina are consistent with previous
descriptions for this species in similar habitats (Magnus
1962; James and Pearse 1969; Chartock 1983; Law
1995). Magnus (1962), in the first detailed study of
surface-film feeding in O. scolopendrina, also noted that
as the depth increased with the incoming tide, the
ophiuroids lifted their arms higher in order to maintain
contact with the surface. Clark (1921, in Ely 1942)
described O. scolopendrina as using three arms for
surface-film feeding, while using the other two to anchor the body in a crevice. Aside from brief bursts of
surface-film feeding, O. scolopendrina also engages in
suspension feeding with arms extended in the water
column, and deposit feeding with arms sweeping the
sediments (Magnus 1962; James and Pearse 1969;
Chartock 1983). Suspension feeding was the primary
feeding mode of O. scolopendrina in our study. Chartock (1983) also noted that ophiuroids at Enewetak
switched to suspension feeding as depth increased with
the incoming tide and surface-film feeding ceased. Deposit feeding was relatively infrequent in our study,
especially around the low tide. In the Red Sea, however, Magnus (1962) observed that sweeping the
substratum was the most common feeding method of
O. scolopendrina during times of still water prior to
surface-film feeding.
A sudden increase in surface-film feeding in O. scolopendrina with the incoming tide suggests an external
trigger associated with this tidal event. A layer of sea
foam, carried by the flooding tidal front, accumulates
organic matter and progressively increases in thickness
and discoloration as it moves shoreward across the reef
platform. In Experiment 2, organic aggregates precipitating from sea foam (collected in a nearshore region of
the platform) triggered surface-film feeding by O. scolopendrina when the foam was introduced to enclosed
arenas. The ophiuroids curled their arms around larger
food particles to bring them to the mouth, a method of
feeding previously noted by Chartock (1983). In
Experiment 1, surface-film feeding occurred in enclosed
arenas that excluded foam, indicating that the presence
of the foam itself, particularly before it becomes heavily
laden with organic material, is not a necessary trigger for
this feeding behaviour.
Water flow is known to stimulate suspension feeding
in many species of ophiuroids (e.g. Pentreath 1970;
Miller et al. 1992; Loo et al. 1996). In Experiment 1
however, the pattern of surface-film feeding activity was
similar in control arenas (open to the ambient tidal flow)
and enclosed arenas (without flow), except for a time lag
in the enclosed ones. The mean depth at which surfacefilm feeding peaked and ended did not vary significantly
between the treatments. This similarity in the pattern of
feeding activity in both treatments suggests that
increasing depth, even in the absence of tidal flow, can
trigger surface-film feeding in O. scolopendrina, and that
feeding ceases once the operative depth is exceeded. The
peak in surface-film feeding occurred at a mean depth of
2.3 cm in Experiment 1, which is about half the modal
arm length of the population (4.3 cm), and feeding
ended at a mean depth of 4 cm as the surface moved
beyond arms’ reach of most ophiuroids. Magnus (1962)
also noted that surface-film feeding in O. scolopendrina
occurred at water depths less than 4–5 cm.
Experiment 2 indicated that surface-film feeding in
O. scolopendrina also can be induced by the introduction
of particles to the water column, without increasing
water flow or depth. The ophiuroids were highly sensitive to small amounts of added sand and carmine particles, despite these having little or no nutritional value.
Magnus (1962) observed similar results when he suspended sand and shavings from his razor on the water
surface during the incoming tide. In Experiment 1, water
percolating up through the porous reef substrate with
the flooding tide may have resuspended fine particles
within the enclosed arenas, although this was not visually detectable. Thus, O. scolopendrina may have responded to increased particle concentrations within the
enclosed arenas in addition to increased depth. These
potentially interacting stimuli could only be isolated
under more controlled conditions in the laboratory.
Surface-film feeding associated with the flooding tide
represents a very limited proportion of the activity
budget of O. scolopendrina. Assuming an average duration of 2 min per tidal cycle (as measured in control
arenas in Experiment 1, Fig. 7b) and two low tides per
day, the daily investment in surface-film feeding may be
as little as 4 min day 1 (=0.3%). In a few localized
microhabitats, water flowing off of the reef allowed some
ophiuroids to also engage in surface-film feeding during
the ebbing tide, but this was relatively infrequent. The
vigour of arm sweeping activity during short bursts of
surface-film feeding suggests a rate of energy expenditure which exceeds that of passive suspension feeding
and deposit feeding. Considering the high organic content of particulate matter associated with surface foam
(43%), the rate of energy acquisition is presumably also
highest during surface-film feeding. Although seston in
the water column over the reef platform has a high organic content (75%), it is a very dilute food source for
suspension feeding (23 mgl 1), and surface sediments
swept during deposit feeding have a low organic content
(5%).
The restricted distribution of O. scolopendrina in the
intertidal zone not only affords the ability to exploit the
nutrient-rich water surface layer but also provides a
refuge from predators that are excluded from these
habitats at low tide. Potential predators of these
ophiuroids include a variety of fish, which frequent
intertidal reef flats at high tide (Law 1995). A large
proportion of ophiuroids throughout the study area had
regenerating arms indicative of fish predation, and
individuals tethered in deeper water off the seaward edge
of reef platform at Tiwi Beach were rapidly consumed
by small wrasses and other reef fish (Scheibling unpublished data). Chartock (1983) discussed feeding and
habitat as possible factors contributing to the adaptive
radiation of the genus Ophiocoma, from predominantly
bottom-feeding species in the subtidal zone, to more
specialized species such as O. scolopendrina in the
intertidal zone. Surface-film feeding in O. scolopendrina
may have evolved in response to reduced predation
pressure in intertidal habitats.
The high population density of O. scolopendrina recorded in our study, and elsewhere in the Indo-Pacific
region, suggests this species represents an important
trophic link in shallow reef ecosystems between producers of particulate organic material (such as corals)
and higher-level consumers that prey on ophiuroids. At
Tiwi Beach, the population of O. scolopendrina spanned
more than 200 m of the 300 m wide reef flat. Given an
average density of ophiuroids across this range of
247 individuals m 2 (Table 2), a 1 m section of flooding
tidal front would pass over 49,400 individuals as it
moved shoreward. Assuming only half the population in
this swath (24,700 individuals) engages in surface-film
feeding (Fig. 4) and each animal uses three arms
(Fig. 2), this gives an estimate of 74,100 arms sweeping
the surface film from every meter of tidal front on a
single flood tide. Furthermore, following this burst of
surface-film feeding, these ophiuroids continue to remove particles suspended in the rising water column, or
deposited on the bottom, throughout the tidal cycle. In
turn, they likely are consumed, either completely or
partially (as arm tips), by fish that forage on the submerged reef flat at high tide. Additional studies that
measure ingestion rates and secondary production of
populations of O. scolopendrina, and losses due to predation, are needed to elucidate this species’ role in reef
trophodynamics. Until such information is available,
estimation of the potential ecological importance of
these ophiuroids remains a matter of ‘‘arm-waving’’.
Acknowledgements We thank Donald Macdonald and the Canadian Field Studies in Africa Program 2000 for enabling us to travel
to Kenya and conduct this research. We are particularly grateful to
Jessica Guidobono, Amanda Lane, Erin Myers, Susanne Pokotylo,
and Carley Watson for their untiring assistance in the field. Two
anonymous reviewers and Bruce Hatcher provided helpful advice
on improving the manuscript. The research was supported by a
Natural Sciences and Engineering Research Council Discovery
Grant to RES.
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