N. paleacea on P. torreyi.
Gansel, J. A.
INTRODUCTION
The geographic range of the Pacific North American surfgrass,
Phyllospadix torreyi (Wats) extends from Oregon doun to Baja California
(Munz and Keck, 1963). A root system consisting of rhizoids anchors
to rocks and coarse sands in the lower intertidal regions. This
position in the intertidal provides a buffer against desiccation and
exposure. Air pockets permeate the P. torreyi blades possibly increasing
internal photosynthetic capacity (Barbour and Radosevich, 1979).
Additionally, these air pockets provide the necessary bouyancy to suspend
the blades as a dynamic forest and prevent entanglement with other bottom
masses. Beneath the water's surface and suspended above the bottom, the
surfgrass blade community offers a reasonably well protected habitat to
any lightweight organism capable of holding on.
The chaffy limpet, Jotoacmea paleacea (Gould), is one archeogastropod
that seems to have responded to this challenge particularly well. Several
major modifications leave N. paleacea ideally adapted to Phyllospadix
species. Conforming in shell width to the width of the blade, N. paleacea
can withdraw all body tissues into its shell to effectively grasp the
blade (lab and field observations). A notch along the right side of the
nuchal cavity coupled with rapid ciliary currents allows water circulation
and waste removal without relinguishing that grasp (Yonge, 1962). Even
defense mechanisms seem centered on remaining in contact with the blades,
Where other small gastropods display mushrooming and abandoning behavior
to avoid predation, I. paleacea simply clamps down tighter and relies on
chemical camouflaging (Fishlyn and Phillips, 1980). Rounding out its
specificity to Phyllospadix species, 1. paleacea also relies on the blades
as a food source.
Parasitism seems to best describe the symbiotic relationship between
Gansel, J. A.
I. paleacea on P. torreyi
Notoacmea paleacea and Phyllospadix torreyi. N. paleacea grazes on the
chlorophyl containing epidermal cell layer of the plant, presumably
lowering the photosynthetic capacity and decreasing blade strength. In
the field, this should result in lessened blade growth rates and decreased
resistance to blade breakage. Aggressive feeding by N. paleacea could
seriously suppress P. torreyi populations. That N. paleacea does not
destroy the P. torreyi populations seems to suggest that some mechanism
exists to control N. paleacea grazing behavior.
Contained within are the results of a study on the symbiotic
relationship between Notoacmea paleacea and Phyllospadix torreyi. Along
with a distribution relating N. paleacea body size to exposure, this paper
examines residency rates on P. torreyi, gut analyses, rates of blade
consumption, and the effects of grazing on photosynthetic capacities of
P. torreyi
METHODS AND RESULTS
Field Studies
To determine a distribution based on degree of exposure to wave
turbulence and desiccation, Notoacmea paleacea were collected from three
sites on the Monterey Peninsula. In order of increasing exposure these
sites include: Bird Rock Channel - Hopkins Marine Station, Stillwater
Cove - Pebble Beach, and West Beach - II.M.S.
Bird Rock Channel refers to the sand and rock bottomed channel
running between Bird Rock and shore. At low minus tides this channel
transforms into a large tide pool with the majority of P. torreyi blades
remaining submerged. At high tide, the area is totally submerged but
strong wave action is broken up by the offshore reef.
Stillwater Cove lies behind a barrier of offshore rocks which create
Gansel, J. A.
II. paleacea on P. torreyi
a natural breakwater. At low minus tides the collection site consists of
numerous shallow tide pools which are succeptable to dessication. At
high tides, the area is submerged and strong surf is again broken up.
Hest Beach has very little protection against strong wave action.
At low minus tides the collection site becomes a channel washed by broken
waves. At high tide, direct wave contact results in a relatively high
energy environment.
Distribution data is presented in figure 1. This data suggests that
N. paleacea body sizes are a function of their environment. Statistically,
(student "T"-test) all mean lengths and mean heights are significantly
different (p £ 0.01) except for length comparisons of Stillwater Cove and
West Beach (0.1 2 p 20.05) and height comparisons of Bird Rock Channel
and West Beach (0.2 2 p 20.1). Statistics suggest that the populations
are overall significantly different in size. This difference corresponds
to the differences observed in wave and desiccative exposure.
Determination of Notoacmea paleacea residency times involved
selectively marking blades of Phyllospadix torreyi with tagged wires.
Observations over a seven day period regarding residency were made on 25
blades chosen for their initial habitation by N. paleacea. Approximate
shell size was also recorded to ensure that the same N. paleacea were
being observed from day to day. All observations for distribution and
field studies took place during spring at low minus tides. Collection
samples included both the residing N. paleacea and the blade occupied.
Data from the blade residency time study appears in figure 2. All
25 blades were occupied by a separate Notoacmea paleacea on day 1 but by
day 2 only 84% (21 of 25) remained occupied. Blade number one represents
a limpet which joined the study after day one. Blades were chosen
because the were occupied by N. paleacea. It was assumed these limpets
Gansel, J. A.
I. paleacea on P. torreyi
represent a random sample with respect to previous time spent on a blade.
Statistically the mean blade residency time for first day occupied blades
is expected to equal half the actual mean residency time. Calculated
from a mean blade residency time for first day occupied blades of 2.88
days, the actual mean blade residency time for N. paleacea on Phyllospadix
torreyi is 5.76 days. This analysis is supported by blade number one
(figure 2). Offering a known beginning and ending time of blade occupancy,
its blade residency time of five days corresponds closely with derived
mean blade residency of 5.76 days. N. paleacea also reappeared on
abandoned P. torreyi blades. The extent of this reoccurrence was always
limited to one observation period.
Rates of consumption of Phyllospadix torreyi by Notoacmea paleacea
were determined in an outside aquarium under natural sunlight in unfiltered
running sea water at 15 + 1° C. Twelve ungrazed blades, each approximately
25 cm long, were suspended on a wooden rack in order to keep them separated.
Collected N. paleacea were transfered to these blades. Lengths and
locations of grazed patches were recorded over the following three day
period. After observations were completed, two 20 cm portions of grazed
and ungrazed blades were dryed overnight and weighed.
Data for consumption rates of Phyllospadix torreyi is presented in
figure 3. Of the initial 12 Notoacmea paleacea, only 8 survived through
the third day. The total length of P. torreyi eaten per day is X - 24.42
mm (S.D. - 19.69) while the length eaten per day considering only the
third day is X - 38.63 mm (S.D. - 14.45). M. paleacea were considered
dead when they dropped from their blades and no jonger exhibited the
ability to reattach. Grazed patches were easy to see and measure. After
the three day observation period, the blades were collected, and dryed.
The difference between 20 cm of grazed plant (0.0324 g) and 20 cm of
Il. paleacea on P. torrey
Gansel, J. A.
ungrazed plant (0.0412 g) gives a value of 0.044 mg per mm of P. torreyi
grazed. Calculations show that 24.42 mm of blade grazed per day corresponds
to a consumption rate of about 1 mg of blade per day or considering the
last day alone, 1.7 mg of blade grazed per day. This gain corresponds to
approximately 1/50 of the wet body weight of an average sized N. paleacea
(8.1 mm, 0.083 g).
Gut samples were analyzed from freshly collected Notoacmea paleacea.
Dissections involved removal of the dorsal half of the shell including
the apex. After the stomach was located and slit open, its content was
removed and transfered to a slide, where it was spread, and finally
mounted in a glucose solution for examination under the compound microscope.
In addition to gut analyses, thin slice cross sections of Phyllospadix
torrevi grazed portions were also mounted and examined under the compound
microscope.
The mounted Phyllospadix torreyi cross sections revealed grazing of
the outer epidermal layer with little or no damage to inner mesophyl
layers. Viewed dorsally and anterior, the stomach was located just to the
right and below the intestine. Its contents were dark green with a few
scattered reflective grains intermixed. Under the compound microscope,
the majority of the stomach contents (approximately 85%) consisted of
P. torreyi cortical cell fragments best characterized by parallel rows of
single layered cells. Some of these fragments still contained chloroplasts.
Far less common (approximately 102), were the two diatom species found.
Finally, in small amounts, fragmented xylem cells were observed. These
cells were identified by the existence of accompanying pit cells. l
The effects of grazing on the photosynthetic rate of Phyllospadix
torreyi were measured on a Gilson respirometer (IGRP-14). Paired samples
composed of equal lengths of grazed and ungrazed P. torreyi were measured
N. paleacea on P. torreyi
Gansel, J. A.
for photosynthetic activity. Each sample was placed in a respirometer
flask under 10 ml of unfiltered sea water and buffered with 1 ml of a
0.035 M. KHCO, and 0.065 M. NaHcO, solution in the side arm of the flask.
The running temperature was set to 15° C., the shaking motor to 5, and
light at the blades was measured at 247 microeinsteins / me : sec. After
allowing for a 20 minute equilibration period, observations were recorded
every 15 minutes for 135 minutes. At the end of the observation period,
the blades were recovered, dryed, and weighed.
After dividing by dry weights, photosynthetic capacity was graphed
in figure 4. Choosing a common period of relatively constant 0,
production, a linear regression was performed over the 30 to 90 minute
interval. Moticably lower slopes indicate a lower photosynthetic rate
for grazed plants. Statistically, the difference between grazed (x -
34.05 ul 09 / g : min, S.D. - 4.02) and ungrazed (50.51 ul 02 / g : min,
S.D. - 1.96) blades is significant (student "T"-test, 0.05 p 0.02).
DISCUSSION
The distribution data in figure 1 suggests that environmental
conditions such as wave intensity and exposure to desiccation piay an
important role in determining the overall body size of Notoacmea paleacea.
As environmental strains increase, N. paleacea size decreases significantly.
The strong wave action at West Beach could be either selectively destroying
larger N. paleacea by selecting against increased drag (increasing size),
or acting against the whole population simply by limiting the average age.
Decreased size at Pebble Beach could be a function of decreased
opportunity grazing activity or some metabolic burden limiting growth,
or again, the hostile environment might simply be lowering the probability
of survivingto reach larger sizes.
Gansel, J. A.
N. paleacea on P. torreyi
That 4 of 12 Notoacmea paleacea (25%) died in the consumption
rate study is probably the result of injuries inflicted during the
transfer process from field to lab Phyllospadix torrevi. Considering a
chance of injury to the surviving N. paleacea, it seems justifiable to
interpret figure 3 by considering day three alone rather than all three
days in determining a mean consumption rate. Day three rates have both
a greater mean (consumed length per day of 38.63 mm compared to 24.42 mm)
and a lower standard deviation (14.45 compared to 19.69). By the third
day, N. paleacea seems to be relatively stable on the lab blades. From
third day data, N. paleacea consumes approximately 1/50 of its own body
weight per day in dry weight of P. torreyi epidermal cells. More
significantly, over a 5.76 day period (mean residency period) this amounts
to a grazing length of 220 mm.
The majority of Phyllospadix torrevi chlorophyl is contained within
the epidermal cell layer. Grazing by Notoacmea paleacea upon the epidermal
cells would be expected to lower photosynthetic capacity. Photorespirometer
results verify this conclusion. Oxygen production is over 30% lower in
grazed blades, indication significantly reduced photosynthetic capacities.
Overgrazing could have a devastating effect on plant growth with such
high rates of photosynthetic loss.
The discovery of xylem cells in gut samples indicates that Notoacmea
paleacea does at least some grazing much deeper than was previously recorded
(Barbour, 1979; Fishlyn, 1980). Grazing deeper than -the epidermal cell
layer should seriously weaken the blade; however, this weakening was not
observed. Deep grazing then probably does not occur often or for long
stretches. In any case, deeper grazing would surely amplify the risks
involved in overgrazing.
Overgrazing certainly threatens the stability of the limpet - surfgrass
N. paleacea on P. torreyi
Gansel, J. A.
relationship. Without controls on the grazing rates of Notoacmea
paleacea, irreparable damage to the P. torreyi population is inevitable.
Evidence towards the existence of such a limiting mechanism is found in
the residency period study (figure 2). Residency periods seem to be of
two types: a full period of residence lasting an average of 5.76 days
and an abbreviated residence time lasting a maximum of one day (actual
abbreviated period is unknown). Itiis suggested that full residency
(5.76 days) indicates an average period the blade is occupied for grazing
while abbreviated residency indicates that the blade was found unsuitable
for grazing. If this is the case, residence on blades by N. paleacea
is not random, but involves a selective process. Perhaps N. paleacea
can recognize recent residency on a blade. The suggested selection
against previously occupied blades would effectively control overgrazing.
Such a mechanism limiting overgrazing is clearly advantagous to
both Phyllospadix torreyi and Notoacmea paleacea. With the extreme
effects of grazing on photosynthetic capacities, overgrazing would be a
serious detriment to the blades. A mechanism limiting grazing ensures
that the P. torreyi population will not be irreparably damaged. Notoacmea
in turn is dependant upon the prosperity of its host Phyllospadix torreyi.
N. paleacea on P. torreyi
Gansel, J. A.
SUMMARY
1. Distribution studies indicate that differences in Notoacmea
paleacea population body sizes correspond to factors of wave intensity
and desiccation from exposure to air.
2. The mean grazing rate on Phyllospadix torrevi is 38.63 mm of
blade length per day or approximately 220 mm over an average grazing
residency of 5.67 days. N. paleacea consumes about 1.7 mg per day dry
weight of P. torreyi.
3. Grazing results in over a 302 loss in photosynthetic capacity.
4. Gut analysis shows P torreyi epidermal cells constitute about
85% of the diet of N. paleacea with small amounts of xylem cells and
diatoms making up the remainder.
5. Periods of residency of individual limpets on blades of
Phyllospadix torrevi may be grouped into two categories: full residency
periods of 5.76 days and abbreviated residency periods of one observation.
6 Full residency periods indicate grazing behavior while
abbreviated residency periods indicate rejection of the blade as a food
source. This points to the existence of a mechanism that enables
N. paleacea to detect previous residency. This mechanism controls
overgrazing, a control that is critical to the success of P. torreyi and
N. paleacea.
N. paleacea on P. torreyi
Gansel, J. A.
ACKNOWLEDGMENTS
I wish to extend special thanks to my advisor CHUCK BAXTER for his
patience and quidance, to Dr. Isabella Abbott for the trifle and help
in analyzing limpet guts, to Robin Burnett for his suggestions on
statistical analysis, and to the rest of the Hopkins staff, and fellow
students for making the quarter so enjoyable. I can't imagine spending
spring anywhere else.
10
N. paleacea on P. torreyi
Gansel, J. A.
LITERATURE CITED
Barbour, Michael G. and Stephen R. Radosevich. 1979. "C Uptake by
the marine angiosperm Phyllospadix scouleri. Amer. J. Bot. 66:
301 - 306.
Fishlyn, Debby A. and David W. Phillips. February 1980. Chemical
camouflaging and behavioral defenses against a predatory seastar
by three species of gastropods from the surfgrass Phyllospadix
community. Biol. Bull. 158:34 -48.
Munz, Phillip A. and David Keck. 1959. A California flora. 1681.pp.;
133 figs.,; Berkeley, Calif. (University of California Press).
Yonge, C. M. 1962. Ciliary currents in the mantle cavity of species of
Acmea. The Veliger 4: 119 -123.
Gansel, J. A.
N. paleacea on P. torreyi
12
FIGURE CAPTIONS
Figure 1. The relation of length and height of 3 populations of Notoacmea
paleacea to increasing levels of exposure. West Beach exposure is
greater than Stillwater Cove exposure is greater than Bird Rock Channe!
exposure.
Figure 2. Residency periods of individual M. paleacea on marked P, tor
blades over a seven day period.
Figure 3. Lengths of grazed areas on Phyllospadix torrevi blades for
individual M. paleacea over a three day period.
Figure 4. Photosynthetic activity graphed against time in minutes for
grazed and ungrazed blades of P. torrevi.
Figure 1
13
BIRD ROCK CHANNEL HMS
TTT

L
STILLWATER COVE PB
II
T
WEST BEACH HMS

T

L
—

6 7 8 9 10 11

3 4
HEIGHT bottom LENGTH top mm.
O
DAYS BLADE HOLDS A LIMPET
N 0
0
14
120
100
80
60
40
.
Figure 3
AFTER DAY
DAY 2
DAY 3


3
limpet number


15
36.8
o


31.2
° 2


ao


2 6
8
49.1

4
0
O
o
0
0
51.8
0
0
0
2
0
o
o


90
120
30
60
minutes
Figure 4
16