factors determining the patchy distribution of the pacific sand dollar

FACTORS DETERMINING THE PATCHY DISTRIBUTION OF THE PACIFIC
SAND DOLLAR, DENDRASTER EXCENTICUS, IN A SUBTIDAL
SAND-BOTTOM HABITAT
A Thesis Presented to the Faculty
of
California State University, Stanislaus
through
Moss Landing Marine Laboratories
In Partial Fulfillment
Of the Requirements for the Degree
Master of Science in Marine Science
By
Tamara Lea Voss
December 2002
DEDICATION
To my family for their constant love and unending support. Thank you.
iii
ACKNOWLEDGMENTS
As with all accomplishments, they are never completed alone. I wish to thank the
Moss Landing Marine Laboratories community, fellow classmates who enthusiastically
offered their help in the field, and their time with in the lab, and the MLML professors
who generously shared their wisdom and experience.
I would like to thank my thesis committee: Drs. Stacy Kim, Kenneth Coale,
Pamela Roe, and Gary Greene for their help and support during my long tenure at
MLML. I especially wish to thank Stacy for her woulderful guidance and patient
compasswn.
The Mary Stewart Rogers Fellowship from California State University,
Stanislaus, provided partial funding for this work.
iv
TABLE OF CONTENTS
PAGE
Dedication.......................................................................................
m
Acknowledgements............................................................................
IV
List of Tables....................................................................................
VI
List of Figures...................................................................................
vn
Abstract... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
vm
Introduction......................................................................................
I
Materials and Methods.........................................................................
9
Results............................................................................................
17
Discussion... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
22
Literature Cited...................................................................................
30
Tables..............................................................................................
36
Figures.............................................................................................
46
Appendix..........................................................................................
53
v
LIST OF TABLES
PAGE
TABLE
I
Sampling schedule including site, date, location, sample type, . . ...
and number of replicates.
36
2
Statistical results for Del Monte Beach core samples.................
37
3
Mean and standard deviation of groupings per core..................
38
4
Statistical results for Coast Guard Jetty core samples................
39
5
Sediment characteristics inside and outside Dendraster excentricus
beds.
40
6
Statistical results for mean grain size, inside versus outside the sand
dollar beds.
41
7
Statistical results for settlement experiments............................
42
8
The mean and standard deviation of Dendraster excentricus.........
larvae that metamorphosed, remained as plutei, or were lost
from the experiment.
43
9
Category groupings that resulted from post-hoc comparisons........
of the settlement experiments
44
vi
LIST OF FIGURES
PAGE
FIGURE
1
Oral and Aboral views of Dendraster excentricus test... . . . . . . . . . . . .
46
2
Dendraster excentricus beds comparing shoreward . . . . . . . . . . . . . . . ...
and seaward edges.
47
3
Perpendicular and parallel alignment of sand dollars within. . . . . . . ..
a bed.
48
4
Competent Echinopluteus of Dendraster excentricus, . . . . . . . . . . . . . . .
showing adult rudiment within larval gut area.
49
5
Aboral view of a newly metamorphosed juvenile . . . . . . . . . . . . . . . . . . ..
Dendraster excentricus.
50
6
Map of Monterey Bay, California showing the location of..........
the two study sites.
51
7
Seasonal adult Dendraster excentricus density at the Del Monte...
Beach site.
52
vii
ABSTRACT
The Pacific sand dollar, Dendraster excentricus, can form dense assemblages in the
shallow sandy subtidal. The distribution of beds of D. excentricus is patchy along the
Pacific coast, and factors controlling the distribution of sand dollars are not well
understood. The distribution of sand dollar beds at two sites within Monterey Bay was
evaluated for infaunal community structure. Infaunal organisms were determined to
belong to one offour groups (burrowers, predators, tube-builders, or Mollusca). These
groups were examined for their effects on one another and on sediment stability, both
inside and outside of the adult sand dollar bed. Additionally, sand dollar plutei that were
competent to metamorphose were offered several substrata to determine what type of
settlement cue is necessary for successful settlement and metamorphosis to take place.
Larviphagy, the cannibalism oflarvae of D. excentricus by its adults, was evaluated as
another factor important in determining initial distribution of sand dollar beds. The
results of the study indicate that the distribution of sand dollar beds are initially
established and maintained by settlement processes.
vi:ii.
INTRODUCTION
Range and Distribution
The Pacific sand dollar, Dendraster excentricus, (Figure 1) is an irregular
echinoid belonging to the Order Clypeasteroida. Patchy beds of D. excentricus exist
from Alaska to Baja California, covering the sand bottoms of both sheltered bays and
open coast areas (Chia, 1969; Merrill & Hobson, 1970; Birkeland & Chia, 1971; Timko,
1975, 1976; Niesen, 1977; Cameron & Rumrill, 1982; Highsmith, 1982). D. excentricus
is found intertidally along its northern distribution and in shallow subtidal waters along
its southern distribution (Chia, 1969; Birkeland & Chia, 1971; Timko, 1975; Niesen,
1977; Cameron & Rumrill, 1982). Subtidal sand dollars live in an inclined position with
their anterior edge partially buried in the sand (Chia, 1969, Timko, 1975, 1976; Smith,
1981; Morin et al., 1985). D. excentricus can form dense aggregations of up to several
hundred individuals per square meter (Chia, 1969; Birkeland & Chia, 1971; Smith, 1981;
Highsmith, 1982; Morin et al., 1985). These beds may exist for decades at the same
location, much longer than the life span of the individuals, which is approximately eight
years (Jensen, 1969; Birkeland & Chia, 1971; Highsmith, 1982).
The shoreward edge of a sand dollar bed seems to remain in the same location on
the bottom throughout the year. Although periods of high surf can temporarily displace
large numbers of sand dollars, the bed margin is reestablished within a few days after the
storm (Morin et al., 1985). The shoreward edge is located where major sand movement
stops, just outside the breaker line. The seaward edge is more distinct than the shoreward
edge (Figure 2). It moves out during the winter until the bed reaches irs peak width in
1
January, when it starts migrating back shoreward (Morin et al., 1985). Pisaster
brevispinus and P. giganteus, seastars that prey on D. excentricus in this environment, are
found along the seaward edge of the sand dollar bed, and may influence its location
(Birkeland & Chia, 1971; Morin et al., 1985).
Habitat
Merrill and Hobson (1970) defmed four habitats that D. excentricus occupies: (1)
bay, (2) tidal channel, (3) protected outer coast, and (4) exposed outer coast. Individuals
of the "bay" type assume a horizontal position, lying flat on the sand or burrowing just
below the surface of the sand. The substratum consists of fme, poorly sorted sand,
usually with an overlying layer of detritus. Most individuals occur in water 0.6 to 1.2
meters deep. During unfavorable conditions, such as exposure during falling tides or
when heavy rains decrease salinity, individuals of D. excentricus will burrow deeper into
the sands rather than move to deeper water.
The "tidal channel" habitat includes strong tidal currents, and clean, well-sorted
sand, with most individuals living in the inclined position. Populations of D. excentricus ·
within tidal channels can be found with either their lateral axis perpendicular to the surge
current (Figure 3a), or parallel to the surge current (Figure 3b). When the sand dollar's
lateral axis is perpendicular to the surge current its oral surface faces upstream, and when
it's lateral axis is parallel to the surge current, its oral surface faces either right or left
across the current.
Sand dollars of the "protected outer coast" maintain an inclined position with
their anterior edge buried in the sand, and align their lateral axis parallel to the strong
2
onshore-offshore sweep of the current surge, which is perpendicular to the weaker long-.
shore transport (Merrill & Hobson, 1970) (Figure 3b ). These beds tend to have sharp
seaward margins, which exhibit the maximum density in 6 to 12 meters of water; the bed
extends shoreward to approximately just outside the breaker line.
Sand dollars of the "exposed outer-coast" are not found close to the shore and are
completely buried (Merrill & Hobson, 1970). According to Merrill and Hobson (1970)
this situation extends north from Point Conception into Oregon and Washington, and less
is known about the individuals found in these locations than those in the other three
habitat types.
Natural History
Dendraster excentricus uses three different methods to feed, depending upon the
type of food being handled. Food items include particles <50J.l1Il, non-motile material,
and motile prey (Timko, 1976). Transportation of particles <50J.l1Il in size toward the
mouth is by ciliary currents. Tube feet are used to grasp and push non-motile material,
>50J.l1Il in size, toward the food grooves. Small active prey are trapped by the spines,
which enclose them, and create a cone-like trap. The large bidentate pedicellariae are
then used to crush the prey before it is placed into the food grooves.
Dendraster excentricus spawning occurs from mid-April through August, during
which time eggs and sperm are shed into the water column where fertilization takes place
(Strathmann, 1987). The larval form is a planktotrophic echinopluteus. Development
takes 3-8 weeks and larvae are competent to metamorphose when the adult rudiment has
3
visible tube feet and spines and fills the larval body (Chia & Burke, 1977; Strathmann,
1987) (Figure 4).
It takes 1-2 hours to complete metamorphosis from a bilaterally
symmetric echinopluteus to a radially symmetric juvenile sand dollar (Figure 5)
(Strathmann, 1987).
Patchiness
The distribution of sand dollar beds is patchy along the Pacific coast. There are
many locations in the shallow, sandy, subtidal environment, some adjacent to standing
beds, that are uninhabited by Dendraster excentricus (Smith, 1981; Highsmith, 1982;
Morin et al., 1985). Patchiness or spatial heterogeneity of D. excentricus beds provides a
unique opportunity to examine if particular shifts in the abundance patterns of infaunal
organisms occur across sand dollar bed boundaries. Sand dollar beds can be created and
maintained by many different mechanisms. Both biological and physical factors have
been used to explain the patchy distribution of sand dollars (Birkeland & Chia, 1971;
Timko, 1975; 1976; Niesen, 1977; Cameron & Rumrill, 1982; Brenchley, 1982; Morin et
al., 1985). From a physical perspective, near-bottom hydrodynamic flow across the bed
is altered, relative to non-settled regions of the seafloor, by the high densities of sand
dollars, and may facilitate filter feeding (Timko, 1975). From a biological perspective,
mass spawning in close proximity may enhance reproductive success, by increasing the
likelihood that eggs and sperm will meet quickly in the water above the beds. Other
biotic causes of patchiness can include differential larval settlement, differential larval
survival, or spatial separation of competitors or between predators and prey (Wilson,
1968; Newell, 1970; Muus, 1973; Meadows & Campbell, 1972; Gray, 1974; Pickett &
4
Cadenasso, 1995). Adults are thought to provide a biochemical cue for settling larvae,
that signals good habitat (Highsmith, 1982). Recruitment success is improved when
larvae settle and metamorphose in a location suitable for adult survival (Caldwell, 1972;
Burke, 1984). The dense numbers of sand dollars in beds may also provide protection
from strong currents by dissipating the energy of the wave surge, or by providing refuge
for the newly metamorphosed juveniles from predation due to adult and predator
interactions (Timko, 1975, 1976; Woodin, 1976, 1978; Highsmith, 1982). Sand dollar
bed formation can also be episodic and therefore temporally variable. The understanding
of where and why beds form is crucial to autecological understanding and predictive
capacity.
Infaunal Community
Biological factors such as competition, predation, adult-larval interactions, and
the re-working of the sediment are well known for the structuring of soft sediment
communities (Woodin, 1974, 1976, 1978; Wiltse, 1980; Smith, 1981; Brenchley, 1982;
Ambrose, 1991; Zajac & Witlatch, 1991). Infaunal organisms found inside the sand
dollar beds may affect Dendraster excentricus by preying on the settling larvae or newly
metamorphosed juveniles. Alternatively, the reworking of the sediment by the infauna
during locomotion and deposit feeding may cause young sand dollars to be buried or
incidentally ingested. On the other hand, dense aggregations of D. excentricus along the
central California coast may play an important role in the stabilization of the soft
sediment communities in that locality. Sand dollar beds may alter the infaunal
community by reducing near bottom current speeds and stabilizing sediments, providing
5
a different habitat than the nearby shifting sand. Whether sand dollar beds in soft
sediment provide habitat that hosts unique communities can be determined by firSt
ascertaining any differences in the infaunal communities found inside and outside the bed
area, and then developing testable hypotheses that explain why these differences occur.
Larval Settlement Cues
Marine invertebrate larvae initiate settlement, and metamorphosis to the juvenile
stage, in response to a variety of cues. Cues may be physical (e.g. substratum rugosity;
Gray, 1974; Crisp, 1974), or biological (e.g. microbial films; Celmer, 1975), and cues
may act as attractants or repellents (Doyle, 1975; Burke, 1984; Woodin, 1991 ). Cues
often act in combination, and interact with other factors such as larval supply and
hydrodynamic flow to defme settlement success (Butman, 1987; Eckman, 1983). For
Dendraster excentricus·there is a small temporal window of opportunity for settlement
and metamorphosis; larvae must first reach a stage in their development in which they are
competent to metamorphose before they will respond to settlement cues. Larvae that
have been competent for too long may settle even in the absence of appropriate cues,
because the larvae do not have enough energy reserves to delay metamorphosis any
longer (Birkeland et al., 1971; Highsmith & Emlet, 1986).
Highsmith (1982) has demonstrated that intertidal adults of Dendraster
excentricus play a beneficial role and signal good habitat for larval settlement and
metamorphosis. Cues released by the adults in the subtidal populations may be
waterborne or sand-bound, or sandy subtidal substratum may be a sufficient textural cue
for settlement and metamorphosis. Differential survival of settlers affects recruitment
6
success, or survival to reproductive age, but the initial distributional pattern is
established by larval settlement.
Larviphagy
Larviphagy, the cannibalism of!arvae by adults, was reported by Timko (1975,
1979) as a density dependent filter of settlement success. Woodin (1976) developed a
hypothesis that predicts that settlement of essentially all larvae, including larvae of their
own species, would be prevented by a high density of suspension feeding adults. If
Iarviphagy occurs given that adults are filter feeders that can ingest settling larvae, adults
of Dendraster excentricus may have a negative role in larval settlement success. Timko
(1975) suggested larviphagy as a mechanism to explain the erratic settlement cycles of
Dendraster excentricus, as described in the literature, by predicting, "only very low
levels of settlement (are) to be expected where adults are abundant and dense." On the
other hand, a successful settlement event would be predicted only when the adult density
has decreased; and space has opened up within the bed. As a result, beds of D.
excentricus should demonstrate age distributions with dominant year classes. Timko
(1975, 1979) carried out Iarviphagy experiments by placing individuals of D. excentricus
with their oral surface up and injecting larvae onto the oral surface of the test using a
syringe with a catheter tube connected to its end. Highsmith (1982), on the other hand,
found that Iarviphagy did not occur during his experiments. He placed larvae in a bowl
with an adult D. excentricus lying with its oral surface down. If the larvae were
competent to metamorphose, they did so. If the larvae contacted the adult they were
eventually rejected by the tube feet lining the food grooves. The major differences
7
between these two works were the position of the adult, either oral side up (not natural)
or oral side down (natural), and the placement of the larvae. Timko placed the larvae on
the oral surface of the adult, whereas, Highsmith added larvae to the adult's bowl and
allowed the larvae to come into contact with the adults on their own. More work using
adults in a normal feeding position is required to answer the question of whether or not
larviphagy occurs, and what effects it might have with respect to larval recruitment in D.
excentricus.
Hypotheses
An initial factor that controls sand dollar bed distribution is settlement success.
Settlement success is an interplay of (1) larval supply, (2) substratum selection and
metamorphosis, and (3) larval or early juvenile mortality, which results in specific
patterns of settlement. The factors influencing larval settlement patterns must first be
better documented and understood so that sand dollar bed patchiness can be explained: I
will examine factors affecting settlement success with a combination of field
observations and laboratory experiments.
The objectives of this study are to:
I.
Provide a description of the infaunal community found within a protected
outer coast sand dollar bed, and assess the potential influence of in faunal
species (e.g. by predation, tube-building or burrowing activities) on sand
dollar recruitment.
2.
Test for differential larval settlement and metamorphosis in response to
various cues from a subtidal sand dollar bed.
3.
Determine if larviphagy occurs in subtidal sand dollars.
8
MATERIALS AND METHODS
Study sites
The fieldwork for this study was conducted along the southern end of Monterey
Bay, California (Figure 6). Two protected outer coast sand dollar beds were investigated
for density of Dendraster excentricus, description of infaunal organisms, and grain size
analysis. The first site was along the Del Monte Beach next to the commercial wharf in
Monterey. The second was located near the Coast Guard Jetty in Monterey. Laboratory
experiments, investigating larval settlement cues, were carried out at the Moss Landing
Marine Laboratories facilities using adults collected from the Del Monte Beach
population.
Del Monte Beach
The sand dollar bed at the Del Monte site is in deep, clean sand located at 36°
36.07' N, 121 o 53.29' W (Figure 6; site 1). No rock outcrops, no attached algae or kelp,
and no drift algae or kelp were observed in over 15 SCUBA dives and several other free
dives. Centimeter size ripple marks were typically present at Del Monte Beach. When
individuals of Dendraster excentricus were buried, they were invisible under the rippled
surface. A diatom film covered the sand by late summer. The bed was protected from
prevailing wind and swell. Its shoreward margin extended to just outside the breaker line
in water depth of 4.5 meters, and was not as distinct as its seaward edge, which ended
abruptly in waters of seven meters depth. Individuals of D. excentricus were inclined on
9
their anterior edge, perpendicular to the beach, and parallel to the surge current (Figure
5b). After storms or rough surge, sand dollars were redistributed, outside their usually
defined beds, or completely buried, but would rapidly reform the bed and return to an
inclined position within a few days.
Coast Guard Jetty
The beach at the Coast Guard Jetty also has a protected outer coast sand dollar
bed. This beach is located at 36° 36.57' N, 121 o 53.62' W (Figure 6; site 2). There are
boulders nearby with attached algae and kelp to the west, and a deep sand channel,
running generally north-south, to the east. There were thick stands of the red alga
Gracilaria sp. within the adult sand dollar bed. Individuals of Dendraster excentricus
were very dense underneath the Gracilaria. The bed was in 5-10 meters of water
(shoreward and seaward edges, respectively). This site was visited twice in August 2001;
individuals of D. excentricus were observed to be inclined and parallel to the surge
current.
Infaunal Description
Samples were taken from inside and outside the adult Dendraster excentricus
beds at both the Del Monte Beach and the Coast Guard jetty sand dollar beds to provide
descriptions of the infaunal community (Appendix A). All biological cores were
collected by myself using SCUBA, which allowed for observation of the D. excentricus
bed and careful sample acquisition. The biological samples were collected using 13 oz
10
coffee cans with both ends removed. The bottom of the can was replaced with tightly
sealed 500Jlm mesh screen and the top had a watertight plastic lid. The samplers had a
diameter of 10 em and length of 15 em (0.008m2). The average depth of a collected core
was 10 em. The samplers were carefully pushed into the sediment. A watertight snap-on
plastic lid was shoved down along side the can until it could be fitted over the opening.
The core was then dug out and the lid checked to make sure it was well sealed. Bed cores
were not taken in areas unoccupied by D. excentricus; in areas of sparse occupation,
cores were taken where there were visible aggregations of D. excentricus. Cores were
also collected from an area outside the adult D. excentricus bed, this was located 5-6
meters seaward of the sand dollar bed. Six cores were taken from each site at each time.
This number of replicates was sufficient for infaunal community evaluation based on data
from other quantitative studies (Hodgson & Nybakken, 1973). Once on shore the
samples were immediately screened with a 500Jlm sieve and all screened organisms were
fixed with 5% buffered formalin in seawater. After 24 hours the formalin was poured
off, the sample was rinsed in fresh water, and stored in 70% alcohol. The animals were
later sorted, identified and counted under a dissecting microscope. Polychaete and
crustacean species were assigned to one of three functional groups: tube-builders, active
burrowers, or predators (Fauchald & Jumars, 1979; Slattery, 1980). Nematodes and
copepods were considered to be representative of meiofauna and were not quantified.
The density of D. excentricus individuals larger than 1em was determined by use
of a 0.25 m 2 quadrat. The quadrat was dropped pseudo-randomly in the bed and all
individuals of D. excentricus within it were counted. This resulted in a pattern of
haphazard, though presumably unbiased, sampling rather than a strictly random one.
11
This was done for practical considerations due to the difficulty in relocating a sand
anchor that would have served as a point of origin, from which a random sampling
pattern could have been set-up. After November 2000, the technique was changed
slightly, and the sediment and animals were scooped out of the quadrat area and screened
underwater through a 1mm sieve. All specimens of D. excentricus were placed into a
sack and brought to the surface, to be counted. This change ensured that the very small
"yearlings" of D. excentricus were not under-counted. Counted sand dollars were
returned to the bed. The density of D. excentricus specimens smaller than 1em was
obtained from the infaunal core samples.
Sediment was analyzed to ascertain any difference between inside and outside the
adult sand dollar beds. A sediment core (diameter 3 em, length 15 em) and its duplicate
were taken at each study site within and outside the bed for analysis. The samples were
first dried and then sieved through a series of seven sieves (2.0mm, 1.0mm, 0.355mm,
0.250mm, 0.180mm, 0.125mm, and 0.090mm), which were placed on a mechanical
shaker for 15 minutes. The fraction retained by each sieve was weighed. Mean grain
size, sorting coefficient, percent silt and clay, and percent and type of debris were
determined (Folk, 1968). Twenty-five sampling events were made from April2000 to
August 2001 (Table 1).
Larval Settlement Selectivity
Larvae of Dendraster excentricus that were competent to metamorphose were
used to evaluate several different substratum cues that might be needed for
metamorphosis to occur. Cues tested included the presence or absence of sand, adults,
12
and an unidentified chemical cue in the sand or water from an adult sand dollar bed.
Larvae for these experiments were spawned in the laboratory from adults collected from
the subtidal bed at the Del Monte Beach site. Eggs and sperm were collected by injecting
sand dollars with 1 mL of 0.5 M KCl periorally. They were then placed aboral surface
down in a small glass dish. Eggs and sperm are easily distinguished. Eggs of D.
excentricus are pale orange, 110-125 fliil in diameter, and are covered by a thick jelly
coat (Strathmann, 1987). This jelly coat contains small peripheral red granules, which
are cells (Strathmann, 1987). One to two drops of sperm were added to the dish
containing the eggs and fertilization was allowed to occur. After approximately 2-3
hours, the fertilized eggs were placed in a large bowl with -1.5 liters of filtered seawater
and the bowl was placed on a wet table in the aquarium room at Moss Landing Marine
Laboratories. After the early pluteus, 2-armed stage was reached, the larvae were divided
into small dishes and fed with Duna/iella every other day. Larval cultures were neither
stirred nor bubbled with air as this causes damage to the developing larvae. Cultures
were maintained on a running seawater table at -15-16°C. The range of time from
spawning to competence was 3-5 weeks. Larval competence to metamorphose was
determined by the presence of the adult rudiment, tube feet, or spines in the larval gut
area (Birkland & Chia, 1971; Highsmith, 1982; Caldwell, 1972). Settlement experiments
involved introducing competent larvae into beakers that contained the various substrata to
be evaluated and scoring their response as '.'metamorphosed," "remained as larvae," or
were "lost from the experiment."
Four different settlement selectivity experiments were run. The experiments
evaluated seven substratum types: (A) filtered seawater, (B) bed seawater, (C) "baked"
13
sand, (D) sand from an adult bed, (E) an adult specimen of D. excentricus only, without
sand of any type, (F) an adult of D. excentricus plus "baked" sand, and (G) an adult of D.
excentricus plus sand from the adult bed. Sand for the settlement experiments was
collected from densely populated areas of the Del Monte Beach bed on the morning the
experiment was to start. Sand from a bed that was to be used for the baked sand
substratum type was collected earlier and baked for 24 hours at 150°C in an oven to
deactivate any chemical cue which might be present. Water for the treatment type that
used bed seawater was taken from an aquarium used as a holding tank for sand dollars
that had contained animals for several weeks prior to the water being used in the
substratum experiments.
For the first experiment, 10 competent larvae were placed in each of 1-liter
beakers containing one of the seven different substratum types being tested. Three
replicates of each substratum were used, for a total of 21 beakers. When the experiments
were terminated, each replicate was fixed with 5% buffered formalin and rose bengal in
seawater. After 24 hours the replicates were rinsed with fresh water, screened with a
250Jlill sieve, and stored in 70% alcohol. With the aid of a dissecting microscope,
replicates were later scored as metamorphosed individuals, larvae still present, or
individuals lost from the experiment. The first experiment testing all seven substrata ran
for 48 hours. The second experiment, also testing all seven substrata, ran for 18 hours
and used five replicates, each with nine competent larvae. The decrease in time between
the first and second experiment was made to ensure that the larvae were not undergoing
metamorphosis simply because they were ready and had reached a "now or never"
period. The time period necessary for metamorphosis was tested by placing two
14
competent larvae in a small dish with an adult. Complete metamorphosis was observed
to take place in approximately three hours; thus, if metamorphosis of competent larvae is
initiated on contact with a suitable cue, an 18-hour time frame should be sufficient for
complete metamorphosis. The third experiment that tested two substrata types using
three replicates with eight larvae each was run for 18 hours. The treatments, selected to
refme the results of the two initial experiments, were (C) baked sand and, (F) D.
excentricus plus baked sand. The fourth experiment compared the treatments (D) bed
sand, (E) D. excentricus only, and (G) D. excentricus plus bed sand, using three replicates
with nine larvae each, and was run for 18 hours.
Larviphagy Experiments
The concept of larviphagy was investigated because of the apparent contradiction
between the larvae returning to an adult bed due to the "signaling" of good habitat by the
adults, and the fact that adults of Dendraster excentricus are filter feeders and have been
reported to consume the returning larvae (Timko, 1975, 1979). Adults of D. excentricus
that had been collected within the week were offered plutei at the 4-arm, 6-arm, or 8-arm
stage. Behavior of the adult and plutei were watched for an hour. After the initial hour
of observation the dishes containing the adult and plutei were placed on the seawater
table and checked again the next day. Adults of D. excentricus were also offered newly
hatched Artemia nauplii that are of similar size as the D. excentricus larvae
(500-750~IDJ).
Additional observations were made using D. excentricus adults that had been held in
aquaria for several weeks and were presumably in a starved condition.
15
Statistical Analysis
Infaunal samples from the Del Monte Beach bed were evaluated for differences
over time and differences between inside and outside the adult Dendraster excentricus
bed. The Coast Guard Jetty study site was evaluated for differences between inside and
outside the adult sand dollar bed. They were evaluated using both ANOVA and t-tests
for differences between three types of functional groups, tube-builders, active burrowers,
and predators as well as differences in the density of Mollusca, the total number of
species, the total number of individuals, and the density of juvenile sand dollars.
Statistical calculations employed the use of SYSTAT I 0.0 (SPSS Inc, 2000). When
necessary, data were ftrst transformed using In ( x+ 1) to correct for homogeneity. If
variances were not homogenous even after data were transformed, a Kruskal-Wallis test
was used.
An ANOVA or t-test was used for larval substratum selectivity experiments. If
the null hypothesis of no difference was rejected, a post-hoc test (Tukey's or
Bonferroni's) was used to make multiple comparisons to determine which of the means
were significantly different from one another. The assumptions of independent data were
addressed by careful experimental design. Homogeneity of variances were evaluated
using the Cochran's test (Winer, 1971) and were calculated by hand. The KolmogorovSmirnov test was used to test for normality of data.
16
RESULTS
Infaunal Cores
Del Monte Beach
When statistical tests were used to test for differences between tube builder,
active burrowers, predators, Mollusca, juvenile sand dollars, total number of species, and
total number of individuals with respect to date and location inside or outside sand dollar
beds (Table 2). There was a significant difference in both time and location for juvenile
sand dollars and for Mollusca, with more juveniles occurring inside the adult bed and
during August 2001 (Table 3). There was a significant difference over time, but not
location, for active burrowers and the number of species present, with more individuals
occuring in the summer (Table 2). There was a significant interaction between time and
location effect for number of species and for the number of individuals, but not for any of
the other groups, indicating that, for total number of species and individuals, the factors
of season and location cannot be separated.
Coast Guard Jetty
When infaunal cores were analyzed for differences between inside and outside the
adult sand dollar bed, using the same groups as in the Del Monte data (Table 4), there
were significantly more active burrowers, juveniles, number of species, and number of
individuals inside than outside the bed (Table 3, 4). There were also significantly more
Mollusca outside the bed (p = 0.026) (Table 4).
17
Grain Size Analysis
There was no significant difference in grain size, sorting value, percent silt and
clay, and percent and type of debris, between inside and outside the adult sand dollar
beds at either of the study sites (Table 5, 6). The sorting value, which is a measure of
standard deviation, for both sites was< 0.35<!1, and falls into the classification of very
well sorted sand. The sediment analysis does not indicate unique characteristics that
designate the presence or absence of D. excentricus, and cannot be used alone to describe
the differences found in the infauna distributions.
Adult Density
Mean densities of Dendraster excentricus were significantly higher at the Coast
Guard Jetty site than at Del Monte Beach for adults larger than I em, measured in 0.25m2
quadrats (224 ± 120 and 7 ± 5 animals per 0.25m2 , respectively,p = 0.001). Adults
ranged from 26 to 405 animals per 0.25m2 at the Coast Guard Jetty study site, and from 1
to 13 animals per 0.25m2 at Del Monte Beach. The density of adult D. excentricus
changed seasonally at the Del Monte site (Figure 7). Seasonal density decreases in the
winter and increases in the summer at the Del Monte site were statistically significant (F
= 2.870,p = 0.015, n = 43).
The decrease in density during the winter when surge was
heavier reflects changes in the areal distribution of the bed rather than fluctuations in the
number of D. excentricus (Morin eta!., 1985).
18
,,:·
~.,,,,
Larval Substrate Selectivity Experiments
When patchiness of the adult Dendraster excentricus bed was tested to determine
if it was the result of differential settlement of larvae, the initial assumptions of
homogeneity of variances and normality of data were supported by results of Cochran's
and Kolmogorov-Smirnov tests, respectively (Table 7).
Experiment 1
In the first experiment, in which seven substrate types were used (Table 8), and
the experiment ran for 48 hours, the ANOVA analysis produced a finding of significance
between the different treatment means (F-ratio = 68.154,p = <0.0005, n = 21). The
treatment results grouped into three different categories: treatments not associated with
adults, treatments associated with adults, and the adult with baked sand treatment, which
grouped by itself (Table 9). The mean of each treatment in a group differs significantly
from every other treatment mean in the other two groups, but does not differ significantly
from the other treatment means within the group.
Experiment 2
In experiment two, which included all seven substrata types and ran for I 8 hours,
the one-way ANOVA analysis of the treatment means showed a significant difference (Fratio= 34.268, p = 0.000, n = 35). Again the means of each treatment in a group differed
significantly from every other treatment mean in the other group, but did not differ
significantly from the other treatment means within the group (Table 9). The resulting
19
groups were similar but not exactly the same as in the first experiment. The treatment
type adult with baked sand grouped with the filtered seawater, bed seawater, and baked
sand treatments. The second group, those treatments associated with adult sand dollars,
remained the same.
Experiment 3
The two-sample t-test was not significant (t = 3.0, p = 0.058, n = 6) in experiment
three, in which only two substrata, baked sand, with and without an adult, were compared
(Table 8). The power of this analysis was 0.764. There are two complications to
interpreting the results of this experiment. The first is that one replicate of the adult with
baked sand treatment type was lost due to the death of the adult during the experiment.
The second observation is that there were more metamorphosed larvae for these two
treatments than in either of the previously run experiments. These larvae were the oldest
(35 days from spawn to date used in an experiment) used, and may have reached their
metamorphosis threshold.
Experiment 4
In the fmal experiment, which compared three substrata, the treatments associated
with adult sand dollars; adult only, bed sand, and adult with bed sand (Table 8) there was
significant difference (F-ratio = 7 .0, p = 0.027, n = 9) shown by the ANOVA. A
Bonferroni post-hoc test determined a significant difference between the adult and adult
20
with bed sand treatments. The other two comparisons were not significantly different
(bed sand, and adult only; bed sand, and adult with bed sand).
Larviphagy
Larvae that added to containers with adults swam around and contacted the spines
and tube feet of the adults, but no adult behavior, such as using the spines to trap the
larvae or extending the pedicellariae to crush larvae, were seen. During two of the trials
involving 8-arm, competent larvae, three individuals were observed to undergo
metamorphosis.
Larvae of early developmental stages (4-arm, 6-arm, and 8-arm pre-competent)
were observed to continue development, comparable to the larvae in the culture dish from
which they had been taken. Fully competent, 8-arm, larvae were found the next day to
either be swimming around or were seen to have completed metamorphosis over night
and the newly metamorphosed juveniles were crawling around on the bottom of the dish.
When larvae of Artemia, (brine shrimp) were added to the dish the adult
immediately reacted by initiating a trapping response with its spines. The tube feet and
pedicellaria also grabbed the brine shrimp larvae, which were rapidly captured, crushed,
and put into food grooves, where they were transported to the oral surface and into the
mouth.
Adults in trials using sand dollar larvae with adults that had been held unfed in
seawater aquaria for several weeks, and were presumed to be starved, displayed spinetrapping and used their tube feet and pedicellaria to capture and place the larvae into their
food grooves.
21
DISCUSSION
The soft-bottom environment of the shallow subtidal is a variable habitat with
strong wave surge and constantly shifting sand. In shallow water, soft sediment stability
is altered by physical disturbances that re-suspend sediment via high-energy wave surge
(Gray, 1974; Ortb, 1977; Eckman, 1983). There are also biological factors that can act to
either stabilize or destabilize the sediment. Sediment stability can be increased by the
tube building activity of small crustaceans and polychaetes (Rhoads & Young, 1971 ).
Sea grasses and other objects can stabilize sediment by buffering currents and damping
wave action (Ortb, 1977). The stability of the sediment can be decreased by burrowing
and deposit feeding activities of the infauna, which rework the sediment (Rhoads &
Young, 1970; Rhoads, 1974).
This soft-bottom shallow water habitat has been recognized as having distinct
community assemblages (Fager, 1968; Merrill & Hobson, 1970; Davis & VanBlaricom,
1978; Oliver et al., 1980; Kastendiek, 1982; VanBlaricom, 1982; Morin et al., 1985),
characterized by low species diversity and density (Dexter, 1969; Day et al., 1971). The
different infaunal communities can alter the physical character of their environment and
thus influence their surrounding community structure by interaction via predation,
competition, and sediment reworking (Woodin, 1974, 1978; Ortb, 1977; Brenchley, 1978,
1981, 1982; Smith, 1981; Highsmith, 1982; Ambrose, 1991). Woodin (1976) described
competitive and trophic interactions of three functional assemblage groups that were
burrowing deposit feeders, suspension feeders, and tube-builders, and explained that the
observed sharp boundaries between assemblage groups were due to interactions among
the established infauna and settling larvae. Burrowers and tube-builders compete for
22
space, with tube-builders binding the sediment and restricting the activity of burrowers.
Burrowers rework the sediments, preventing survival of tube-builders, and increasing the
re-suspension of sediments which 'clogs' the filters of suspension feeders, and ingest the
settling larvae of both groups. Suspension feeders filter all the groups' larvae from the
water column, inhibiting successful settlement. Thus the autecology and abundance of
benthic organisms interact with and influence the community and habitat structure.
Brenchley (1981) experimentally demonstrated a significant reduction in tube-builder
density after the addition of active burrowers ( Upogebia pugettensis, Abarenicola
pacifica, and Dendraster excentricus).
In the intertidal, Dendraster excentricus destabilizes sediments by burrowing into
the sediment at low tide to prevent desiccation, and inclining at high tide to filter feed.
The sediment destabilization due to intertidal sand dollars leads to significantly more
tube-builders outside sand dollar beds, and significantly more active burrowers inside the
beds (Smith, 1981; Brenchley, 1978, 1981). In addition, Smith (1981) found lower
species diversity inside intertidal sand dollar beds, indicating that fewer species were able
to coexist with intertidal D. excentricus.
Though intertidal sand dollars destabilize the sands through their burrowing
activities, subtidal sand dollars may stabilize shifting sand and allow infaunal organisms'
access to this high-energy area. Because subtidal sand dollars do not bury and incline
with each tidal cycle like intertidal sand dollars do, there is a less dramatic reworking of
the sediments by the subtidal sand dollars. This resulted in less disturbance, and even
enhances habitat stability. Sediment stabilization by a single species can play a major
role in structuring the community (Kim, I 989). My results of no significant difference in
23
abundance of tube-builders or active burrowers inside or outside the Del Monte sand
dollar bed support my prediction of little or no sediment-reworking disturbance within
the bed. Evidence for increased stability in subtidal D. excentricus beds is demonstrated
by the significantly higher number of species and individuals observed inside the bed
than outside the sand dollar bed at the Coast Guard Jetty. Mollusks, mostly sedentary,
were significantly higher outside the bed at both study sites. This was an expected
pattern due to the competitive interactions between sedentary suspension feeders and
active burrowers, as described by Woodin (1976).
Smith ( 1981) listed the infaunal species found inside and outside intertidal sand
dollar beds and indicated just one species that occurred in only one location. The tubebuilding amphipod Ampe/isca agassizi occurred solely outside sand dollar beds. All
other organisms had varied abundances but were found inside and outside sand dollar
beds in at least one of the 10 sites studied. The subtidal sand dollar beds investigated by
Merrill and Hobson ( 1970) also shows no animals endemic to sand dollar beds, but many
organisms were recurrent and were regarded as characteristic. Merrill and Hobson
(1970) hypothesized that subtidal sand dollars not only stabilize the substratum by
curtailing the erosion of sand in this high-energy environment but also provide refuge
from predation. I also found no species endemic to the subtidal sand dollar beds studied
(Appendix A). The species lists of organisms found inside and outside the bed were
similar and differed only in the abundances of the organisms.
24
Substratum Selectivity
Settlement, the influx of the youngest age class, is an important mechanism
shaping the structure of a population (Cameron & Schroeter, 1980). The understanding
of Dendraster excentricus bed patchiness is improved with the increased knowledge of
sand dollar larval settlement. Larval settlement in response to a specific cue has been
determined for several marine invertebrates (Crisp, 1974; Cameron & Hinegardner, 1974:
Gray, 1974), and recruitment success is improved when larvae settle and metamorphose
in a location suitable for adult survival (Caldwell, 1972; Highsmith, 1982; Burke, 1983).
Settlement cues can include far field signals like waterborne chemicals, temperature or
light, and near field signals that may be tactile such as substrate rugosity or grain size, or
chemical contact signals from conspecifics, prey, or biofilms (Crisp, 1974; Celmer, 1975;
Chia & Burke, 1977; Burke, 1983; Highsmith, 1982; Butman, 1987; Woodin, 1991).
Larvae of intertidal Dendraster excentricus are known to settle and metamorphose in the
presence of adults of the species (Caldwell, 1972; Highsmith, 1982). It is believed that a
chemical cue is released by adults of D. excentricus and is sequestered in the sand of the
bed. The results of the current subtidal study were similar. Greater larval metamorphosis
occurred in treatments associated with adults. Highsmith's (1982) results with intertidal
sand dollars determined that the greatest metamorphosis occurred in response to the adult
only treatment. The subtidal work showed the greatest metamorphosis occurring in the
bed sand treatment (experiment 1) and adult with bed sand treatment (experiment 2). The
25
adult only treatment was second, for both experiments. Although the presence of the
adult is important in providing the chemical cue and thereby conditioning the sand, what
appears to be more important for triggering metamorphosis in larvae is the presence of
conditioned sand. The different results for the adult with baked sand treatment between
the first two experiments leads to the further question of how long it takes for an adult to
condition the sand. Although the length of time the experiments were allowed to run was
shortened to 18 hours after the first experiment of 48 hours as a precaution for larvae
reaching the "now or never" stage, this did not end up being a concern, but led to the
discovery of a potential time factor in which the sand must be exposed to the adults for
the concentration to reach a level sufficient for the larvae to detect, settle, and
metamorphose. The shorter time in the second experiment (18 hours vs. 48 hours) was
evidently insufficient for the adult to introduce the settling cue into the sand. This
indicates that the chemical cue released by the adult is held in the sand, a more localized
cue for a settlement response than if it were released into the water column.
Additionally, the sand itself may provide a physical substratum that the metamorphosing
larval can "hold on to" as metamorphosis occurs. Cameron and Hinegardner (1974)
showed that larvae of Arbacia punctulata are induced to metamorphose by a combination
of a soluble chemical cue and tactile stimulation of the primary podia of the adult
rudiment.
Extrapolation of these results suggests that there should be more settlement and
metamorphosis of larvae inside an existing adult D. excentricus bed than outside of the
bed. For both study sites, Del Monte Beach and Coast Guard Jetty, there were
significantly more newly metamorphosed juveniles inside the bed than outside the bed as
26
determined by the infaunal core data. These results were independent of the different
mean densities of adults within the beds; Coast Guard Jetty had a higher density of sand
dollars than the bed at Del Monte Beach. Larval substratum selection is an initial
controlling factor for the establishment of the stabilizing species, Dendraster excentricus,
in this community. This is an important first order process in understanding the
patchiness of adult sand dollar beds.
Larviphagy
The third objective of this study was to determine iflarviphagy occurs in subtidal
sand dollars. Results from this study indicate that larviphagy does not occur under normal
conditions. If the adults are in a starved condition then larviphagy may occur. This
differs from Timko's (1975) research indicating that larviphagy acted as a density
regulator within the beds. Because sand dollar larvae metamorphose is in response to
conditioned sand within the sand dollar beds, and is not dependent on contact with the
adults, larval mortality due to larviphagy even during conditions that are poor for the
adults, may be low.
Although this work did not address the question of exclusion of infaunal or
epifaunal predators from the sand dollar bed, this would be an area of further study, and
some preliminary predictions based on this and earlier work can be made. Though
differences were not significant, there were more predators inside the bed at both study
sites; most of these were active burrowers. Infaunal predators, if they were active
burrowers, would probably not be excluded from the bed, but if they were sedentary or
tube-builders (such as Leptochelia dubia; Highsmith, 1982), there would probably be
27
negative adult D. excentricus-predator interactions. Epifaunal predators, such as
Pisaster brevispinus, would have difficulty maintaining traction on top of the dense sand
dollar bed in high surge because of the inclined position of the sand dollars. P.
brevispinus would have to make forays into the bed to feed, and retreat when surge
increased.
Within this study there were no unique physical characteristics that explained the
presence or absence of D. excentricus. It has been determined that the adult-conditioned
sand is important in triggering oflarval metamorphosis. In addition, sand grains
probably provide a physical substratum for the larvae to hold on to during
metamorphosis. If so, it is reasonable to assume that there would be a minimum and
maximum grain size in which the larvae's ability to effectively anchor themselves is lost.
To understand the patchy distribution of Dendraster excentricus beds along the
Pacific coast it is necessary to first understand recruitment processes and factors
influencing settlement. A population's recruitment will be determined by larval supply,
substratum selection and metamorphosis (settlement), and early juvenile mortality. From
this settlement study, it was determined that, observed sand dollar bed patchiness is
maintained by larval response to both the presence of adults and adult-conditioned sand
as suitable settlement cues. There were no significant differences in predator abundance
within the beds and outside the beds, and no occurrence oflarviphagy. This indicates
that at these two subtidal sites, the early juvenile mortality pressures were the same inside
and outside the bed. The numbers of newly metamorphosed juvenile sand dollars found
inside versus outside the sand dollar beds were significantly higher at both sites. The
28
results of this study indicate that patchiness of D. excentricus beds are maintained by
settlement processes.
29
LITERATURE CITED
LITERATURE CITED
Ambrose, W. G. 1991. Are infaunal predators important in structuring marine
soft-bottom communities? Amer. Zoo!. 31:849-860.
Birkeland, C., and F. Chia. 1971. Recruitment risk, growth, age and predation in two
populations of sand dollars, Dendraster excentricus (Eschscholtz). J. Exp. Mar.
Bioi. Ecol. 6:265-278.
Birkeland, C., F. Chia, and R. R. Strathmann. 1971. Develpment, substratum selection,
delay of metamorphosis and growth in the seastar, Mediaster aequalis (Stimpson).
Bioi. Bull. 141:99-108.
Brenchley, G. A. 1978. On the Regulation of Marine Infaunal Assemblages at the
Morphological Level: A Study of the Interactions Between Sediment Stabilizers,
Destabilizers, and Their Sedimentay Environment Ph. D. Dissertation, John
Hopkins University, Baltimore. 249 pp.
Brenchley, G. A. 1981. Disturbance and community structure: an experimental study of
bioturbation in marine soft-bottom environments. Journal of Marine Research
39(4):767-790.
Brenchley, G. A. 1982. Mechanisms of spatial competition in marine soft-bottom
communities. J. Exp. Mar. Bioi. Ecol. 60:17-33.
Burke, R. D. 1983. Neural control of metamorphosis inDendraster excentricus. Bioi.
Bull. 164:176-188.
Burke, R. D. 1984. Pheromonal control of metamorphosis in the Pacific sand dollar,
Dendraster excentricus. Science 225:442-443.
Butman, C. A. 1987. Larval settlement of soft-sediment invertebrates: The spatial scales
of pattern explained by active habitat selection and the emerging role of
hydrodynamical processes. Oceanogr. Mar. Bioi. Ann. Rev. 25:113-165.
Caldwell, J. W. 1972. Development, Metamorphosis, and Substrate Selection of the
Larvae of the Sand Dollar, Mellita quinquesperforata (Leske, 1778). M. Sc.
Thesis, University of Florida, Gainsville. 63 pp.
Cameron, R. A., and R. T. Hinegardner. 1974. Initiation of metamorphosis in laboratory
cultured sea urchins. Bioi. Bull. 146: 335-342.
30
Cameron, R. A., and S. S. Rumri11.1982. Larval abundance and recruitment of the sand
dollar Dendraster excentricus in Monterey Bay, California, USA. Marine
Biology 71:197-202.
Cameron, R. A., and S. C. Schroeter. 1980. Sea urchin recruitment: Effect of substrate
selection on Juvenile Distribution. Mar. Ecol. Prog. Ser. 2:243-247.
Celmer, T. 1975c Some observations of three populations of Dedraster excentricus
(Eschscholtz) and their aggregative behavior. Zoology Report 533b, Friday
Harbor Laboratories, San Juan Island, Washington. 19 pp.
Chia, F. 1969. Some observations on the locomotion and feeding of the sand dollar,
Dendraster excentricus (Eschscholtz). J. Exp. Mar. Bioi. Ecol. 3:162-170.
Chia, F., and R. D. Burke. 1977. Echinoderm metamorphosis: Fate oflarval structures.
Pages 219-234 in F.S. Chia and M. E. Rice, editors. Settlement and
Metamorphosis of Marine Invertebrate Larvae. Elsevier, New York.
Crisp, D. J. 1974. Factors influencing the settlement of marine invertebrate larvae. Pages
177-265 in P. T. Grant and A.M. Mackie, editors. Chemoreception in Marine
Organisms. Academic Press, New York.
Davis, N., and G. R. VanBlaricom. 1978. Spatial and temporal heterogeneity in a sand
bottom epifaunal community of invertebrates in shallow water. Limnol.
Oceanogr. 23(3):417-427.
Day, J. H., J. G. Field, and M. Montgomery. 1971. The use of numerical methods to
determine the distribution of the benthic fauna across the continental shelf of
North Carolina. J. Anirn. Ecol. 40:93-126.
Dexter, D. M. 1969. Structure of an intertidal sandy-beach community in North Carolina.
Chesapeake Sci. 10:93-98.
Doyle, R. W. 1975. Settlement of planktonic larvae: A theory of habitat selection in
varying environments. American Naturalist 109(966):1 13-126.
Eckman, J. E. 1983. Hydrodynamic processes affecting benthic recruitment. Limnol.
Oceanogr. 28(2):241-257.
Fager, E. W. 1968. A sand-bottom epifaunal community of invertebrates in shallow
water. Lirnnol. Oceanogr. 13:448-464.
Fauchald, K., and P. A. Jumars. 1979. The diet of worms: A study ofpolchaete feeding
guilds. Oceanogr. Mar. Bioi. Ann. Rev. 17:193-284.
Folk, R. L. 1968. Petrology of Sedimentary Rocks. University of Texas. 170 pp.
31
Gray, J. S. 1974. Animal-sediment relationships. Oceanogr. Mar. Bioi. Ann. Rev. 12:223261.
Highsmith, R. C. 1982. Induced settlement and metamorphosis of sand dollar
(Dendraster excentricus) larvae in predator-free sites: Adult sand dollar beds.
Ecology 63(2):329-337.
Highsmith, R. C., and R. B. Emlet. 1986. Delayed metamorphosis: effect on growth and
survival of juvenile sand dollars (Echinoidea: Clypeateroida). Bulletin of Marine
Science 39(2):347-361.
Hodgson, A. T., and J. W. Nybakken. 1973. A quantitative survey of the benthic infauna
of Northern Monterey Bay, California. Moss Landing Marine Laboratories
Technical Publications# 40:73-78.
Jensen, M. 1969. Age determination ofechinoids. Sarsia 37:41-44.
Kastendiek, J. E. 1982. Factors determining the distributionof the sea pansy, Renilla
kollikkeri, in a subtidal sand-bottom habitat. Oecologia 52:340-347.
Kim, S. L. 1989. The Structure and Organization of a Kelp Forest Ecotone: The Diopatra
ornata Community. M. Sc. Thesis, San Jose State University. 38 pp.
Meadows, P. S., and J. I. Campbell. 1972. Habitat selection by aquatic invertebrates.
Adv. Mar. Bioi. 10:271-382.
Merrill, R. J., and E. S. Hobson. 1970. Field observations of Dendraster excenticus, a
sand dollar of Western North America. The American Midland Naturalist
83(2):595-624.
Morin, J. G., J. E. Kastendiek, A. Harrington, and N. Davis. 1985. Organizaton and
patterns of interactions in a subtidal sand community on an exposed coast. Mar.
Ecol. Prog. Ser. 27:163-185.
Muus, K. 1973. Settling, growth and mortality of young bivalves in the Oresund. Ophelia
12:79-116.
Newell, R. C. 1970. Biology oflntertidal Animals. Paul Elek Ltd.
Niesen, T. M. 1977. Reproductive cycles in two populations ofthe pacific sand dollar
Dendraster excentricus. Marine Biology 42:65-373.
32
Oliver, J. S., P. N. Slattery, L. W. Hulberg, and J. W. Nybakken. 1980. Relationships
between wave distrubance and zonation of benthic invertebrate communities
along a subtidal high-energy beach in Monterey Bay, California. Fishery Bulletin
78(2):437-454.
Ortb, R. J. 1977. The importance of sediment stability in seagrass communities. Pages
281-300 in B. C. Coull, editor. Ecology of Marine Benthos. University of South
Carolina. Columbia, South Carolina.
Pickett, S. T. A., and M. L. Cadenasso. 1995. Landscape ecology: Spatial Heterogeneity
in ecological systems. Science 269:331-334.
Rhoads, D. C. 1974. Organism-sediment relations on the muddy sea floor. Oceanogr.
Mar. Bioi. Ann. Rev. 12:263-300.
Rhoads, D. C., and D. K. Young. 1970. The influence of deposit feeding benthos on
bottom stability and community trophic structure. Journal of Marine Research
28:150-178.
Rhoads, D. C., and D. K. Young. 1971. Animal-sediment relations in Cape Cod Bay,
Massachusetts. II. Reworking by Molpadia oo/itica (Holothuroidea). Mar. Bioi.
11:255-261.
Slattery, P. N. 1980. Ecology and Life Histories of Dominant Infaunal Crustaceans
Inhabiting the Subtidal High Energy Beach at Moss Landing, California. M. S.
Thesis, San Jose State University. 114 pp.
Smith, A. L. 1981. Comparisom ofmacrofaunal invertebrates in sand dollar (Dendraster
excentricus) bed and in adjacent areas free of sand dollars. Marine Biology
65:191-198.
Strathmann, M. F. 1987. Reproduction and Development of Marine Invertebrates of the
Northern Pacific Coast: Data and Methods for the Study of Eggs, Embroys, and
Larvae. University of Washington Press. Seattle. 670 pp.
Timko, P. L. 1975. High Density Aggregation in Dendraster excentricus (Eschscholtz):
Analysis of Strategies and Benefits Concerning Growth, Age Structure, Feeding,
Hydrodynamics and Reproduction. Ph. D. Dissertation, University of California,
Los Angeles. 305 pp.
Timko, P. L. 1976. Sand dollars as suspension feeders: A new description offeeding in
Dendraster excentricus. Bioi. Bull. 151:247-259.
33
Timko, P. L. 1979. Larviphagy and oophagy in benthic invertebrates: A demonstration
for Dendraster excentricus (Echinoidea). Pages 91-98 inS. E. Stancyk, editor.
Reproductive Ecology of Marine Invertebrates. University of South Carolina
Press, Columbia, South Carolina, USA.
VanBlaricom, G. R. 1982. Experimental analyses of structural regulation in a marine
sand community exposed to oceanic swell. Ecological Monographs 52(3):283305.
Wilson, D.P. 1968. The settlement behavior of the larvae of Sabellaria alveolata. J. Mar.
Bioi. Ass. U.K. 48:378-435.
Wiltse, J. R. 1980. Effects of Polinices duplicatus (Gastropoda: Naticidea) on infaunal
community structure at Barnstable Harbor, Massachusetts, USA. Mar. Bioi.
56:301-310.
Winer, B. J. 1971. Statistical Principles in Experimental Design. McGraw-Hill Book .
Company.
Woodin, S. A. 1974. Polychaete abundance patterns in a marine soft-sediment
environment: the importance of biological interactions. Ecological Monographs
44:171-187.
Woodin, S. A. 1976. Adult-Larval interactions in dense infaunal assemblages: Patterns of
abundance. Journal of Marine Research 34:25-41.
Woodin, S. A. 1978. Refuges, disturbance and community structure: a marine softbottom example. Ecology 59:274-284.
Woodin, S. A. 1991. Recruitment ofinfauna: Positive or negative cues? Arner. Zoo!.
31:797-807.
Zajac, R.N., and R. B. Whitlatch. 1991. Demoraphic aspects of marine, soft sediment
patch dynamics. Arner. Zoo!. 31:808-820.
34
TABLES
Table I. Sampling schedule including site, date, location, sample type, and number ofreplicates,
collected for each type of analysis. Location refers to either inside the sand dollar bed or outside of it.
Live Dendraster or Bed Sand refers to when adults or sandfrom the adult bed were collected to be used in
the larval settlement exe.eriments.
Live Dendraster
Quadrat
Collection Date Location
lnfaunal Core
or Bed Sand
Grain Size
Stud~ Site
Del Monte Beach
4/21/00
Inside
Del Monte Beach
5/6/00
Inside
n =4
Del Monte Beach
7/19/00
Inside
n =3
Del Monte Beach
8115/00
lnside
Del Monte Beach
8/30/00
Inside
Del Monte Beach
10117/00
Inside
Del Monte Beach
I 1/6/00
Inside
IJ
= 4*
Del Monte Beach
2/6/01
Inside
IJ
= 4*
Del Monte Beach
4/24/01
Inside
IJ
= 4*
Del Monte Beach
6113/01
Inside
Del Monte Beach
6/20/01
Inside
Del Monte Beach
7/7/01
Inside
Del Monte Beach
8/9/01
Inside
Del Monte Beach
8/23/01
Inside
n > 20 indiv.
Del Monte Beach
9118/01
Inside
bed sand
Del Monte Bench
I 0/8/01
Inside
bed sand
Del Monte Beach
10/24/01
Inside
bed sand
Del Monte Beach
8113/00
Outside
1l
Del Monte Beach
6/20/01
Outside
n =5
Del Monte Beach
6/13/01
Outside
Del Monte Beach
8/9/01
Outside
n =3
Coast Guard Jetty
8/7/01
Inside
n =6
Coast Guard Jetty
8/14/01
Inside
1J
= 4*
Coast Guard Jetty
8/24/0 I
Inside
1l
= 4*
Coast Guard Jetty
8/24/01
Outside
n = 3
n =6
core
samples lost
core
samples lost
n =5
n =9
n =2
n =4
n =4*
n > 40 indiv.
& bed sand
n =6
n = 6*
=6
1l =
n =6
36
1l
2
=2
n =2
Table 2. Statistical results for Del Monte Beach core samples. A two way ANOVA was pe1jormed on each grouping.
Collection dates a/August 13 and 15, 2000 were analyzed as the same date. Significance at the p ~ 0. 05 level is indicated by *.
In Cochran's test, critical values greater than observed values indicates variances are homogeneous. In Kolmogorov-Smimov's
test p > 0.05 indicates data are normal. For Mollusca and Number of Individuals, data were transformed using In (x +I)
prior to analyses to correct for homogeneity. Kruskai-Wallis test was used for active burrowers because variances were
heterogeneous even after transformation.
Groupings
'"'
o,-J
Time effect
~
~o.ou*
p
~0.175
~0.634
p
~
p
Active burrowers
p
Predators
p
Mollusca
Juveniles of
Dendraster
excentricus
p
~
p
No. of Species
p
p
0.061
p
~
Tube-builders
No. oflndividuals
Location effect
0.060
Interaction effect
p
~0.190
N/A
Cochran's Test
observed critical
0.3914
N/A
0.4447
KolmogorovSmirnov's Test
p
N/A
~
0.061
N/A
0.079
p
~
0.095
0.4307
0.4447
p
~0.811
0.000*
p~0.021*
p
~
0.545
0.3484
0.4447
p
~0.181
~
0.007*
p
0.000*
p
~
0.183
0.3456
0.4447
p
~0.905
~
0.000*
p
~
0.698
p
~
0.038*
0.4212
0.4447
p
~0.831
0.056
p
~
0.936
p
~
0.036*
0.3778
0.4447
p
~0.652
~
~
•.
. ''[~
-"~-,
Table 3. Mean and standard deviation of indivuiduals per grouping per core (0. 008m2).
Study
Site
Del Monte Beach
Collection
Location
Date
Inside
No. of
Tube
Builders
Active
Burrowers
Predators
Mollusca
Juveniles
SEE·
No. of
indiv.
4/21/00
0.33 ± 0.58
n =3
87.33 ± 84.48
n =3
6!.67± 76.16
n =3
2.67 ± 2.52
n =3
2.33 ± 2.52
n =3
10.67 ± 4.51
n =3
148.00 ± 16!.93
n =3
5.83 ± 1!.86
n =6
35.83 ± 19.94
n =6
0.00
n=6
4.50± 4.09
n =6
4.17 ± 2.14
ll = 6
38.17 ± 20.88
n =6
Del Monte Beach
Inside
8115/00
0.50 ± 0.84
n =6
Del Monte Beach
Inside
6/20101
1.25 ± 0.50
n =4
9.25 ± 10.63
n =4
16.75 ± 14.29
n =4
0.00
n =4
7.25 ±4.65
n =4
3.50 ± !.29
n =4
16.75 ± 14.29
n =4
Del Monte Beach
Inside
819101
0.83 ± 1.33
n =6
8.17 ± 4.54
n =6
42.17 ± 26.11
n =6
!.67 ± !.21
n =6
13.00±4.86
n =6
1!.50 ± 3.27
n =6
60.33 ± 3!.37
n =6
Del Monte Beach
Outside
8113100
0.50 ± !.22
n =6
2.67 ± 2.73
n =6
20.67± 12.16
n =6
0.33 ± 0.82
n =6
0.50± 0.84
n =6
4.33 ± 2.07
n =6
22.17±12.51
n = 6
Del Monte Beach
Outside
6120101
2.00 ± 2.35
n = 5
6.60 ±4.04
n =5
25.4 ± 1!.89
n =5
0.80 ± 0.45
n =5
0.80 ± 1.30
n =5
6.80 ± 1.10
n =5
34.80 ± 10.06
n =5
Del Monte Beach
Outside
819/01
3.33 ± 2.08
n =3
20.33 ± 8.33
n =3
13.00 ± 5.29
n =3
2.67 ± 2.08
n =3
3.00± 2.00
n =3
9.00 ± !.73
n =3
40.7± 15.31
n =3
Coast Guard Jetty
Inside
817101
1.17±1.17
n =6
10.00 ± 4.15
n =6
9.83 ± 7.36
n =6
l.OO ± 0.89
n =6
14.33 ± 6.59
n =6
9.17 ± 3.66
n =6
2!.50 ± 7.23
n =6
Coast Guard Jetty
Outside
8/24101
2.30 ± !.86
n =6
1.17 ± 0.98
n =6
4.17 ± 3.60
n =6
3.50± 2.17
n =6
l.OO ± 0.89
n =6
4.50 ± 1.5 2
n =6
10.. 67 ± 3.67
n =6
w
00
r
!
Table 4. Statistical results for Coast Guard .Jetty core samples. A t-test was
performed on each grouping. Significance at the p ~ 0. 05 level is indicated
by *. In Cochran's test, critical greater than observed indicates variances are
homogeneous. In Kolmogorov- Smirnov's test p > 0.05 indicates data are
normal. For Active burrowers and Juveniles, data were transformed using
In ( x + !) prior to analyses to correct for homogeneity.
Groupings
p value
Cochran's Test
Kolmogorov-
observed
critical
Smirnov's Test
Tube-builders
0.223
0. 7172
0.8772
p
~0.818
Active burrowers
0.000*
0.5106
0.8772
p
~
0.423
Predators
0.121
0.8068
0.8772
p
~
0.582
Mollusca
0.026*
0.8545
0.8772
p
~
0.737
Juveniles of
Dendraster excentricus
0.000*
0.5312
0.8772
p
~0.796
No. of Species
0.016*
0.8532
0.8772
p
~0.638
No. oflndivuals
0.008*
0.7952
0.8772
p =0.945
39
···~·~·~··~~··~·~~
.•...
lf•i!l,,
Table 5. Sediment characteristics inside and outside beds of Dendraster excentricus, at both study sites (Del!vfante and Coast Guard Jetty).
Study Site
m
,_
0
sorting value (phi)
mean grain size (phi)
out
m
%silt & clay
out
% debris (broken shells)
m
out
in
out
Del Monte
2.025 ± 0.007 2.015 ± 0.007 0.235 ± 0.007 0.250 ± 0.000
0.00 ± 0.00
0.00 ± 0.00
0.00 ± 0.00
0.00 ± 0.00
Coast Guard Jetty
1.940 ± 0.014 1.920 ± 0.014 0.340 ± 0.000 0.345 ± 0.007
1.28 ± 0.09
1.15 ± 0.07
1.22 ± 0.06
1.05 ± 0.07
...,,,fij;,
••vw···
Table 6. Statistical results for mean grain si:::e, in versus out. A t-test was pe1jormedjor each study site.
In Cochran's test, critical greater than observed indicates variances are homogeneous. In Kolmogorov-Smirnov's
test p > 0. 05 indicates data are normal.
Kolmogorov-
observed
critical
Smimov's Test
p value
t -Statistic
n
Del Monte Beach
0.293
1.414
2
0
0.9985
p =0.999
Coast Guard Jetty
0.293
1.414
2
0
0.9985
p = 0.999
Study site
..,.,_.
Cochran's Test
3',
Table 7. Statistical results for settlement expeiments. Significance at the p = 0.05 level is indicated by*.
In Cochran's test, critical greater than observed indicates variances are homogeneous. In KolmogorovSmirnov~s test p > 0.05 indicates data are normal.
Cochran's Test
observed critical
Kolmogorov-Smimov's Test
Experiment
p value
Statistic
11
Experiment I
0.000*
F =68.154
3
0.5386
0.5612
p = 0.251
Experiment 2
0.000*
F = 34.268
5
0.3546
0.4307
p =0.353
Experiment 3
0.058
t = 3.000
3
0.6667
0.975
p =0.999
0.027*
F =7.000
3
0.7779
0.8709
p
~ Experiment 4
·= 0.266
Table 8. The mean and standard deviation oflan,ae of Dendraster excentricus
that metamorphosed, remained as plutei, or were lost fi'om the experiment.
Experiment I
Treatment type
Metamorphosed
Plutei
Lost
Time (hrs)
Filtered seawater
Bed seawater
Baked sand
Bed sand
Adult only
Adult & baked sand
Adult & bed sand
0.00 ± 0.00
0.67 ± 0.58
0.33 ± 0.33
8.00 ± 0.00
7.67 ± 0.58
3.00 ± 1.00
7.67 ± 1.53
10.00 ± 0.00
9.33 ± 0.58
9.33 ± 0.58
1.67 ± 0.58
2.33 ± 0.58
6.33 ± 0.58
1.67 ± !.53
0.00 ± 0.00
0.00 ± 0.00
0.33 ± 0.58
0.33 ± 0.58
0.00 ± 0.00
0.67 ± 0.58
0.67 ± 0.58
48
48
48
48
48
48
48
Experiment 2
Treatment type
Metamorphosed
Plutei
Lost
Time (hrs)
Filtered seawater
Bed seawater
Baked sand
Bed sand
Adult only
Adult & baked sand
Adult & bed sand
0.40 ± 0.54
0.60 ± 0.55
0.00 ± 0.00
5.60 ± 1.14
3.00±0.71
0.00 ± 0.00
6.20 ± 1.92
8.60 ± 0.55
8.40 ± 0.55
8.40 ± 0.55
3.00 ± 1.41
5.80 ± 0.84
7.80 ± 1.10
2.40 ± 1.52
0.00± 0.00
0.00 ± 0.00
0.60 ± 0.55
0.40 ± 0.55
0.20 ± 0.45
0.40 ± 0.55
0.40 ± 0.55
18
18
18
18
18
18
18
Experiment 3
Treatment type
Metamorphosed
Plutei
Lost
Time (hrs)
Baked sand
Adult & baked sand
5.00 ± 1.00
6.00 ± 2.65
3.00 ± 1.00
1.33 ± 1.53
0.00 ± 0.00
0.67 ± 1.15
18
18
Experiment 4
Treatment type
Bed sand
Adult only
Adult & bed sand
Metamorphosed
5.33 ± 0.58
4.33 ± 1.53
7.33 ± 0.58
Plutei
3.33 ± 0.58
4.67 ± 1.53
1.00 ± 0.00
Lost
0.33 ± 0.58
0.00 ± 0.00
0.67 ± 0.58
Time (hrs)
18
18
18
43
Table 9. Category groupings that resulredji·om post-hoc comparisons
of the settlement experiments.
Experiment I
Group A
Filtered seawater
Bed seawater
Baked sand
GroupB
Groupe
Adult & baked sand Bed sand
Adult only
Adult & bed sand
Experiment 2
Group A
Filtered seawater
Bed seawater
Baked sand
Adult & baked sand
Group C
Bed sand
Adult only
Adult & bed sand
44
FIGURES
Mouth
Oral surface
Petaloid ambulacra
Ocular plate
plate
~Ambulacrum
./
'-
/
Genital pore
........_
'-
/ ,Z.....Jnterambulacrum
Madreporite
Aboral surface
Figure I. Oral aud aboral views of the test of Dendraster excentricus. Figure modified
from Nybakken, West Coast Invertebrate Laboratory Manual, West Coast edition, with
permission from the artist, Lyun McMasters.
46
.
~-"~"~~-"" ""-,~-~-
""'-'
,__,----"" ""'"" ""_,__
" -" ~"-----"-''"""--"~
--~~~---'
Seaward Edge
Shoreward Edge
1
_,_, ____""""-~-~~--"~~" --""-~'-"-----" "~-------~1
\
Open Bay
Shore
Figure 2_ Beds of Dendraster excentricus comparing shoreward and seaward edges. The shoreward edge (left) is less distinct,
compared to the "piled-on" effect at the seaward edge (right).
47
A) Perpendicular alignment
Seaward edge
Shore
B) Parallel alignment
Seaward edge
Shore
Figure 3. Alignment of Dendraster excentricus within an inclined bed. Straight edge
denotes oral surface and convext edge denotes aboral surface. A) Perpendicular
alignment of sand dollars to the surge current, with oral surface facing upstream. B)
Parallel alignment of sand dollars to the surge current, with oral surface facing right or
left with respect to long-shore transport.
48
Adult rudiment
Adult spines
500um
Figure 4. Competent echinopluteus of Dendraster excentricus, showing adult rudiment
within the larval gut area. Total length oflarvae- 750um.
49
500um
Figure 5. Aboral view of newly metamorphosed juvenile of Dendraster excentricus.
50
Santa Cruz
t
. .
I 10 Kilometers I
Pacific Ocean
400
0
Meters
BOO
Site 1
•
Monterey
Figure 6. Map of Monterey Bay, California, showing the location of the two study sites.
Site I is Del Monte Beach. Site 2 is Coast Guard Jetty Beach.
51
Seasonal adult density
40
35 -
N
30 -
E
1£)
f"! 25 -
~
I..
Cl.l
Ln
'"
c. 20 -
-;;"'
= 15 -
"1:1
·;:
·"1:1
=
·- 10
5
0-r-----~-------,-------,-------,------,-------,-------,-------,-----~
5/6/00
7/19/00
8/30/00
10/17/00
11/6/00
2/6/01
4/24/01
Sample date
Figure 7. Seasonal density of adults of Dendraster excentricus at the Del Monte Beach site.
6/20/01
8/9/01
APPENDIX
Appendix A: A list of the number of organisms per taxon per core (.008m2). DM =Del Monte beach, CG =Coast Guard Jetty,
IN = inside sand dollar bed, and OUT = outside the sand dollar bed. Life Stratagies were determined to fit into one of four types;
b = burrowers, p = predators, t = tube builders, or und = undetermined
Core I Core 2 Core 3 Core 4 Core 5 Core 6
Life Strat Organism
Study Site Location Date
b
b,p
b,p
p
Crustacea
Euphilomedes longiseta
Mandibuloplzoxus gi/esi
Rlzepoxynius lucubrans
Synchelidium shoemakeri
DM
DM
DM
DM
IN
IN
IN
IN
4/21100
4/21/00
4/21100
4/21100
55
118
6
24
18
4
0
0
29
23
2
8
b
p
b
t
b
p
Polychaeta
Armandia brevis
Hessionella complex
Mage/ana sacculata
Apoprionospio pygmaea
Scolop/os sp.
Typosyllis sp.
DM
DM
DM
DM
DM
DM
IN
IN
IN
IN
IN
IN
4/21100
4/21/00
4/21100
4/21/00
4/21/00
4/21100
I
3
2
1
0
12
0
0
3
1
0
p
b
Other Worm Groups
Nemertea (Cerebratu/us)
Oligochaeta
DM
DM
IN
IN
4/21100
4/21100
I
I
Mollusca
Tel/ina bodegensis
Rochefortia sp.
0/ivel/a bip/icata
DM
OM
DM
IN
IN
IN
4/21/00
4/21/00
4/21/00
3
und
und
und
7
1
0
0
I
I
0
2
0
0
2
und
Echinodermata
Dendraster excentricus
DM
IN
4/21/00
12
I
9
b
b,p
b,p
p
Crustacea
Euphilomedes longise/a
Mandibulophoxus gilesi
Rhepoxynius lucubrans
Synche/idium shoemakeri
DM
DM
DM
DM
OUT
OUT
OUT
OUT
8113/00
8/13/00
8/13/00
8/13/00
0
0
0
0
I
0
2
3
0
I
5
3
0
0
Nephtys californiensis
Phyl/odoce sp.
Apoprionospio pygmaea
Typosyllis sp.
DM
DM
DM
DM
DM
DM
OUT
OUT
OUT
OUT
OUT
OUT
8/13/00
8/13/00
8/13/00
8/13/00
8/13/00
8/13/00
0
0
I
0
0
I
0
0
0
0
0
II
und
Mollusca
0/ive//a bip/ica/a
DM
OUT
8/13/00
0
und
Echinodermata
Dendraster excentricus
DM
OUT
8/13/00
b
und
b,p
p
Crustacea
Euphilomedes /ongiseta
Juvenile Mysid
Mandibulophoxus gi/esi
Synchelidium shoemakeri
DM
DM
DM
DM
IN
IN
IN
IN
8/15/00
8/15/00
8/15/00
8/15/00
t
p
b,p
p
p
Polychaeta
Capitellidae
Hessionel/a complex
0
I
I
I
0
I
0
0
I
0
0
23
0
0
0
6
I
12
0
0
2
6
0
14
0
0
0
18
0
4
0
I
0
11
0
0
2
0
0
3
I
0
3
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
8
2
0
19
4
0
0
0
I
DM
DM
DM
DM
DM
IN
IN
IN
IN
IN
8115/00
8/15/00
8/15/00
8/15/00
8/15/00
I
4
0
0
5
0
26
I
0
5
0
30
0
0
0
0
68
0
0
0
0
15
I
2
0
0
24
p
Polychaeta
Dispio uncinata
Hessionel/a complex
Nephtys californiensis
Apoprionospio pygmaea
Typosyl/is sp.
p
b
Other Worm Groups
Nemertea (Cerebratulus)
Oligochaeta
DM
DM
IN
IN
8/15/00
8/15/00
0
0
0
I
0
I
2
I
I
0
I
0
NONE
DM
IN
8/15/00
und
Echinodermata
Dendraster excentricus ·
DM
IN
8/15/00
0
0
0
0
I
2
und
b, p
p
t, p
Crustacea
Anchico/orus occidenta/is
Mandibu/ophoxus gilesi
Synchelidium shoemakeri
Zeuxo normanii
DM
DM
DM
DM
IN
IN
IN
IN
6/21/01
6/21101
6/21/01
6/21101
I
22
0
2
0
I
I
I
0
14
15
I
0
0
2
I
t
p
b,p
(
0
5
Mollusca
p
Polychaeta
Hessionella complex
DM
IN
6/2I/OI
3
2
I
0
p
Other Worm Groups
Nemertea (Cerebratulus)
DM
IN
6/21101
0
I
0
0
NONE
DM
IN
6/2I/OI
und
Echinodermata
Dendraster excentricus
DM
IN
6/21/01
0
5
2
0
und
und
b
b,p
b, p
p
Crustacea
Anchicolorus occidentalis
Diastylopsis tenuis
Euphilomedes longiseta
Mandibulophoxus gilesi
Rhepoxynius lucubrans
Synchelidium shoemakeri
DM
DM
DM
DM
DM
DM
OUT
OUT
OUT
OUT
OUT
OUT
6/21/01
6/21/01
6/21101
6121/0I
6/21101
6/21101
0
0
3
0
2
0
0
0
12
0
0
I
3
2
3
1
0
I
0
0
3
0
0
I
0
0
2
0
2
2
Polychaeta
Armandia brevis
Chaetozone sp.
Haploscoloplos sp.
Hessionella complex
Mage/ana sacculata
Apoprionospio pygmaea
DM
DM
DM
DM
DM
DM
OUT
OUT
OUT
OUT
OUT
OUT
6/21/0I
6/2I/OI
6/2110I
6/21/01
6/2I/01
6/2110I
I
0
0
I2
I
0
0
I
0
I3
0
6
0
0
0
24
0
2
0
0
0
43
0
1
0
0
Mollusca
b
b
b
p
b
t
23
0
I
·······~
Other Wonn Groups
Nemertea (Cerebratulus)
Oligochaeta
DM
DM
OUT
OUT
6/21/01
6/21/01
I
I
I
0
0
0
0
0
0
0
und
und
Mollusca
Tel/ina bodegensis
Nassarius perpinguis
OM
OM
OUT
OUT
6/21/01
6/21/01
0
0
I
0
I
0
I
0
0
I
und
Echinodennata
Dendraster excentricus
DM
OUT
6/21/01
3
0
0
0
I
und
t
und
b
b,p
p
und
Crustacea
Anchicolorus occidentalis
Callianassa sp
Cyclaspis sp.
Euphilomedes longiseta
Rhepoxynius lucubrans
Synchelidium shoemakeri
Megaluropus longimarus
OM
DM
OM
OM
OM
OM
OM
IN
IN
8/9/01
8/9/01
8/9/01
8/9/01
8/9/0 I
8/9/01
8/9/01
0
0
0
0
2
4
0
0
0
0
7
0
I
0
0
0
0
0
0
4
0
I
2
I
I
I
4
0
0
0
0
3
0
5
0
0
0
0
2
I
4
I
t
b
b,p
p
b
b,p
und
Polychaeta
Dispio uncinata
Armandia brevis
Glycera sp.
Hessionella complex
Magelona sacculata
Nephtys californiensis
Opheliidae
OM
OM
OM
OM
DM
OM
OM
IN
8/9/01
8/9/01
8/9/01
8/9/01
8/9/01
8/9/01
8/9/01
2
9
0
19
0
0
0
0
0
0
86
0
3
0
0
I
0
17
0
0
0
I
3
0
41
0
0
2
0
4
0
20
0
0
2
0
9
I
32
I
0
9
p
b
IN
IN
IN
IN
IN
IN
IN
IN
IN
IN
IN
·······~
Phyllodoce sp.
Protodrilus!Saccocirrus
Spionidae
Thalenessa sp.
OM
OM
OM
OM
IN
IN
IN
IN
8/9/01
8/9/01
8/9/01
8/9/01
1
0
0
0
0
4
0
I
0
0
I
0
0
2
0
3
0
1
0
0
0
1
0
Other Worm Groups
Nemertea (Cerebratulus)
OM
IN
8/9/01
I
0
0
0
0
I
und
und
und
und
und
und
und
Mollusca
Tel/ina bodegensis
0/ivel/a bip/icata
Naticidae
Tresus -like
Modiolus sp.
Simomactra planulata
Nassarius fossa/us
OM
OM
OM
OM
OM
OM
OM
IN
IN
IN
IN
IN
IN
8/9/01
8/9/01
8/9/01
8/9/01
8/9/01
8/9/01
8/9/01
2
0
0
0
0
0
0
0
0
0
1
0
0
2
0
0
0
0
0
I
0
I
0
0
0
0
0
0
0
1
I
0
I
0
0
0
0
0
0
0
0
0
und
Echinodermata
Dendraster excentricus
OM
IN
8/9/0 I
IS
6
II
10
19
17
b
t
b,p
p
und
Crustacea
Euphilomedes longiseta
Pinnb:a occidentalis
Rhepoxynius lucubrans
Synchelidium shoemakeri
Megaluropus longimarus
OM
OM
OM
OM
OM
OUT
OUT
OUT
OUT
OUT
8/9/0 I
8/9/01
8/9/01
8/9/01
8/9/01
0
0
0
0
0
0
0
I
0
I
p
und
und
p
p
Polychaeta
IN
1
0
I
0
'''''""'~~
b,p
b
p
b
t
b
p
Glycera sp.
Hap/oscoloplos sp.
Hessionel/a complex
Magelona sacculata
Apoprionospio pygmaea
I
2
I2
2
8
IO
8/9/01
8/9/0I
8/9/01
2
I
4
0
I
24
9
5
20
0
3
0
OUT
8/9/0I
I
3
2
DM
DM
DM
DM
OUT
OUT
OUT
OUT
8/9/0I
8/9/0I
8/9/0I
8/9/0I
I
0
I
0
3
I
I
0
0
0
0
DM
OUT
8/9/0I
II3
I2
73
CG
CG
CG
CG
CG
IN
IN
IN
IN
IN
8/7/01
8/7/0I
8/7/01
8/7/0I
8/7/0I
0
0
0
I
0
0
0
0
0
0
I
0
CG
IN
8/7/0I
5
14
OUT
OUT
OUT
OUT
OUT
OUT
8/9/0 I
8/9/01
8/9/01
Opheliidae
DM
DM
DM
DM
DM
DM
Other Worm Groups
Nemertea (Cerebratu/us)
DM
Mollusca
und
und
und
und
Tel/ina bodegensis
Olivella biplicata
Simomactra planulata
Macoma sp.
Echinodermata
und
Dendraster excentricus
und
und
und
b,p
Cyc/aspis sp.
Crustacea
p
Juvenile Mysid
Paraeurystheus sp.
Rhepoxynius lucubrans
Synchelidium shoemakeri
0
2
I
0
0
I
I
8
0
2
0
I
2
0
0
0
0
IO
7
2
I
IO
Polychaeta
b
Armandia brevis
'~
co
IN
IN
IN
IN
IN
IN
IN
IN
IN
IN
IN
IN
IN
IN
IN
8/7/01
8/7/0 l
8/7/01
8/7/01
8/7/01
8/7/01
8/7/01
8/7/01
8/7/01
8/7/01
8/7/01
8/7/01
8/7/01
8/7/01
8/7/01
CG
IN
IN
und
und
und
und
Mollusca
Tel/ina bodegens is
0/ivel/a biplicata
Trachycardium sp.
Naticidae
CG
CG
CG
CG
und
Echinodermata
Dendraster excentricus
CG
b
b
b,p
p
p
b
t
b,p
t
b
p
t
p
p
und
p
b
C/1aetozone sp.
Cirratulus/Tharyx sp.
Glycera sp.
Gyptis sp.
Hessionel/a complex
Magelona sacculata
Mediomastus sp.
Nephtys californiensis
Nereidae
Orbinia or Orbiniidae?
Phyllodoce sp.
Apoprionospio pygmaea
Typosyllis sp.
Pi/argis berkeleyi
Unknown Poly
Other Warm Groups
Nemertea (Cerebratulus)
Oligochaeta
CG
CG
CG
CG
CG
CG
CG
CG
CG
CG
CG
CG
CG
CG
co
0
2
0
I
0
I
0
0
I
I
0
0
20
l
0
0
0
0
0
0
0
0
0
0
0
I
0
0
0
0
0
0
0
0
I
0
0
I
0
I
I
0
0
0
I
0
0
0
0
0
0
0
0
0
0
0
2
0
I
I
I
2
0
0
0
0
0
0
0
0
8/7/01
8/7/01
0
0
0
0
0
0
IN
IN
IN
IN
8/7/01
8/7/01
8/7/01
8/7/01
0
I
I
I
0
0
0
0
0
0
IN
8/7/01
18
9
I
2
I
0
2
0
0
2
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
I
I
I
0
0
0
0
0
0
0
I
0
0
0
0
6
12
17
24
.,JI
Crustacea
und
p
Lamprops sp.
Synchelidium shoemakeri
CG
CG
OUT
OUT
8/24/01
8/24/01
0
2
0
2
0
2
0
I
0
I
I
9
b
t
b,p
b
t
p
p
Armandia brevis
Glycera americana
Mage/ana sacculata
Apoprionospio pygmaea
Thalenessa sp.
Typosyllis s p.
CG
CG
CG
CG
CG
CG
CG
OUT
OUT
OUT
OUT
OUT
OUT
OUT
8/24/01
8/24/01
8/24/01
8/24/01
8/24/01
8/24/01
8/24/01
0
4
0
I
I
0
I
0
0
3
0
I
0
0
0
0
I
0
2
0
0
0
I
0
0
I
0
0
I
I
0
0
I
I
0
0
0
0
I
0
Other Worm Groups
Nemertea (Cerebratulus)
CG
OUT
8/24/01
0
0
0
0
0
3
CG
CG
CG
CG
OUT
OUT
OUT
OUT
8/24/01
8/24/01
8/24/01
8/24/01
0
2
0
I
I
6
0
0
0
0
0
I
0
5
0
0
0
0
2
0
0
3
0
0
CG
OUT
8/24/01
0
I
I
2
0
2
Polychaeta
p
Capitellidae
3
0
Mollusca
und
und
und
und
Tel/ina bodegensis
0/ivel/a biplicata
Simomactra p/anulata
Saxidomus nuttal/i
und
Dendraster excentricus
Echinodermata