INTRODUCTION
For many years investigators have been studying the
mechanisms involved in the penetration of hard shells by
boring organisms (Hancock, 1848; Lindsay, 1912; Hunter, 1949;
Smith, 1969); however evaluating the shell damage done by the
commensal activity has had little work. The many species
of California abalones (Haliotidae) are bored principally
by two animals that live commensally on the shells: Clione
celata Grant, var californiana De Laubenfels, 1932, a boring
sponge (Porifera); and Penitella conradi Valenciennes, 1846,
a boring clam. Cliona celata californiana bores a spreading
network of tunnels in its host's shell as it grows (MacGinitie
and MacGinitie, 1949). The boring piddock, Penitella conradi,
belongs to a group of rock and shell borers of the family
Pholadidae and chemically excavates a burrow which it enlarges
as it grows (Jaccarini, Bannister and Micallef, 1968). This
paper reports on investigations on geographic distribution of
the commensals, the structural damage to host shells, some
aspects of the relationship over historical time, and some
other observations on the biology of this infection. The
main question revolves around the strength of the shell when
infected and the loss of protection against predators. It
is known that sea otters use rocks to break the abalone shell
(Kenyon, 1959) and crabs prey upon the abalone by breaking
off the sides of the shell (Lox, 1962). It was found in this
study that the shell is definitely weaker if it is infected.
MATERIALS AND METHODS
Field and Study Sites
Collection of the many different species of abalones was
from the entire coast of California (fig. 1). A total of 257
shells of Haliotis rufescens, 65 of H. cracherodii, 64 of H.
corrugata, 15 of H. assimilis, 51 of H. sorenseni, and 75 of
H. fulgens were used in the study. As the map indicates the
geographical distribution covered abalones found as far north
as Point Saint George (Latitude 42°, Longitude 124°) and as
far south as the Islas Coronados (Latitute 32°, Longitude
117°). Shells used in the lab experiments were measured for
height (dorso-ventral axis) and maximum length. However only
the amount of infection and the lengths were measured for the
shells not used in the lab studies.
Lab Studies
Many methods were used to find the approixmate amount of
infection of Cliona celata and Penitella conradi to the abalone
shells. When looking strictly at the surface area of the
shell, detection of Penitella was reserved to counting holes
on the outside and the blister pearls on the inside. To
increase accuracy in many cases the shell was cleaned off of
any plant material and sanded in order to show the tip of the
Penitella. For Cliona,shell infection was quantified by
placing a l cm" grid over the surface area and counting the
infected and uninfected squares over the entire surface to
compute the percentage. These were the methods used in a
study on these commensals by Hansen (1970). The above methods
do not take into account the extent of shell damage. Cliona
can bore very deeply into a shell or it can bore only in the
prismatic layer; however, the appearance is equivalent on the
surface area. The Penitella can be large or small and their
pattern of distribution in the shell will affect the amount
of structural damage. Since the borers remove shell material
and the amount of damage is a function of the shell removed:
it was judged that a determination of shell density would be
a good criterion of harm done by these commensals. In the
study 25 Haliotis rufescens shells were cut into 2.5 um wide
strips perpendicular to the longitudinal body axis. The
volume of each strip was calculated by measuring as carefully
as possible the average width, length and thickness. The
weight was also recorded. The density was obtained by
dividing the weight by the volume. The density of an entire
shell was found by averaging the densities of all the strips,
Independent measurements on the same strips indicated an
error of less than + 38.
The first strength test (Fig. 3) estimated the breaking
point while increasing the force applied to a 1 cm rod
resting on the convex surface while the shell was resting
on a scale. The force at which the shell shattered was
recorded. Shells of approximately equal dimensions were used.
The second strength test (Fig. 6) recorded the force at which
individual stripsbroke, when a spring balance was attached
4 centimeters from one end of the strip, while the other end
was fixed. The force was applied horizontally until the strip
broke and the maximum value recorded.
Shells dated as far back as 3500 years by archaeologists
were also looked at. Abalone and fresh abalone shells with
and without commensals were maintained in aquaria with running
sea water. Every 3 days the shells were checked for the
activity of the borers.
RESULTS
Figures 1 and 2 present the collection sites of the 6
species of Haliotis along with the infection rates which
were determined for the two commensals. Cliona is most pre¬
valent in the red abalone with lowest infection in the black
and pink abalones. For Penitella the infection rate is
dramatically lower for the black and somewhat reduced for the
white and threaded abalones.
The tests for strength of the infected shells are pre¬
sented in Figures 3 through 9. Figure 4 shows a correlation
between the breaking force and the amount of surface area
bored by Cliona. High values of boring reduce the strength
of the shell by over 603. The results for Penitella show no
clear correlation between number of Penitella per shell and
breaking point. These are presented in Figure 5 and the graph
reveals the scatter is very wide throughout the range of
infection.
When the strips are tested for their breaking strength
we see a similar relationship as obtained in the whole shells
for Cliona (Figure 7). The slope of the line is similar
indicating a similar reduction in breaking strengh of the
shell strips as a function of percent infection by Cliona.
Figure 8 shows the results of these tests applied to strips
of shell bored by Penitella. Here, though the correlation be¬
tween number of Penitella per shell and breaking strength
does exist, it shows a low slope and a good deal of scatter.
Measuring the density of shell strips revealed a strong
correlation between density and infection. In a shell with
minimal damage by borers the density was 2.78 gms/cm while
another with extensive damage by Cliona had a density of 1.49
gms/cm’. When the force required to break strips was plotted
against shell density there is a very good positive correla¬
tion. Shell of maximal density requires 758 greater force
than those which have been heavily bored and are about 653
of normal density.
DISCUSSION
There exists a good correlation between the damage done
by shell borers and the strength of abalone shells. These
differ between the pholad and sponge since the pholad pro¬
duces localized points of weakness and the sponge progressively
spreads and deteriorates the shell with time. The older
larger shells often have sustained massive damage and offer
little protection to the abalone. There can be little
question that this damage can make them more susceptible to
predation by crabs and otters. An attempt was made to deter¬
mine if a higher proportion of abalone taken by sea otters
had boring damage but the sample was too small to yield con¬
clusive results.
There is a difference in the susceptibility of the
different species of abalone to attack by the borers. The
black abalone which lives primarily intertidally and in the
shallow subtidal has an appreciably lower infection rate for
both Cliona and Penitella. This is perhaps mediated through
habitat difference. The shells are in general quite clean of
growth of algae or other invertebrates. There may be some
depth limitation of Penitella infection as the white abalone
which occupies the deepest waters has the lowest infection
rate of any of the subtidal species.
These two commensals differ in their specificity of host
selection. Cliona can be found associated with a wide variety
of calcareous substrates including shells of oysters, rock
scallops, barnacles, coralline algae and a variety of other
gastropods. Penitella conradi is only reported from abalone.
It would be interesting to see if the infection rate of
Penitella was significantly dropping in the areas where sea
otters forage and have reduced both the population size and
size distribution of abalone. This would require collection
of a large sample of abalone which was not possible.
Many large abalone are taken which do have massive shell
damage by borers and appear to do well in their habitat.
These are in general from outside the range of the sea otter.
Their principal predator which would have to breech the
defense would be large crabs. Since the shell is laid down
at the margins this would provide new strong shell where the
crab would focus its attack.
The activity of boring commensals has been demonstrated
to greatly weaken the shell of abalone. It is still difficult
to quantify what impact this has on abalone survival in
natural situations.
SUMMARY
1. There are direct positive correlations between infection
by shell borers, shell density and the breaking point of
abalone shells.
2. Cliona celata bores into all species studied with the
greatest infection in H. rufesens and the least in H.
cracherodii.
3. Penitella conradi has lowest infection rates in H.
cracherodii and highest rates in H. rufesens, H. fulgens and
H. corrugata.
4. Penitella and Cliona have distinct boring patterns
and damage the shell in different ways.
LITERATURE CITED
Cox, Keith W. 1962. California Abalones, Family Haliotidae.
Fish Bulletin 118, Calif. Dept. Fish and Game,
Sacramento, Calif.
Ebert, Earl E. 1973. Mariculture in California. Calif.
Dept. of Fish and Game, Marine Resources Report No. 18.
Sacramento, Calif.
Hancock, A. 1848. On the boring of the Mollusca into rocks
and the removal of portions of their shells. Ann. Mag.
Natur. Hist. 2: 225-247.
Hansen, John. 1970. Commensal activity as a function of age
in two species of California abalones. Veliger, Volume
13:1.
Hunter, R. 1959. The structure and behavior of Hiatella
gallicana (Lamarck) with special references to the boring
habits. Proc. Roy. Soc. Edinburgh 63: 271-289.
Jaccarini, V., W. H. Bannister and H. Micallef. 1968. The
pallial glands and rock boring in Lithophaga lithophaga.
J. Zool. 154: 397-401.
Kenyon, T. 1970. The sea otter in the eastern Pacific Ocean.
U.S. Bureau of Sport Fisheries and Wild Life. Seattle,
Washington.
Lindsay, B. 1912. On the boring Mollusca of St. Andrews.
Ann. Mag. Natur. Hist. 9: 369-374.
MacGinitie, G.E. Eber and N. MacGinitie. 1949. Natural
history of marine animals. McGraw-Hill, New York.
Meredith, Steven Edward. 1968. Notes on the extension of
the boring clam, Penitella conradi. Veliger 10(3);
281-282.
Moffet, A. 1978. Review of the fishery biology of abalones.
Washington State Dept. of Fisheries. Olympia, Washing-
ton.
Smith, Edmund H. 1969. Functional morphology of Penitella
conradi relative to shell penetration. Am. Zoologist
9: 869-880.
Figure 1
Distribution of Cliona celata californiana in California
abalone. The map on the left shows the latitudinal range
of each spedies; the circles on the lines indicate the
collection spots during the study. The lines are also
arranged in accordance to the depths, where each species
occurs. The bar graph on the right represents the number
of shells being infected by Cliona celata and the 2 surface
area being bored. The data for the figures of depth and
latitude from Cox (1962) and McAllister (1976).
n - the total number of abalones found during the study
o - the specific spot on the latitudinal range where the
abalone was collected
x - the actual geographic spot on the map. The numbers
stand for:
1 - Pt. St. George
2 - Fort Ross
Bodega Bay
4 - Half Moon Bay
5 - Monterey
Pt. Conception
Santa Cruz Is.
8 -
Santa Rosa Is.
9 -
Santa Catalina
10 - La Jolla
11 - Islas Coronadas
Black - Haliotis cracherodii (Leach, 1817)
Red - Haliotis rufescens (Swainson, 1822)
Pink - Haliotis corrugata (Gray, 1828)
Threaded - Haliotis assimilis (Dall, 1878)
Green - Haliotis fulgens (Phillippi, 1845)
White - Haliotis sorenseni (Bartsch, 1940)
Figure 2
Figure 3
Figure 4
Distribution of Penitella conradi in abalones in California.
The same rules apply for this graph as the previous on, and
the legend should be followed identically. The y-axis is
however on a different scale; instead of figuring out the
percentage bored by Penitella conradi, the actual number of
Penitella on the shell was considered. There is a correction
to be made as all three specimens of Haliotis fulgens (Green)
which are indicated to have twenty Penitella per shell
actually had 27, 32, and 45 Penitella respectively for each
of the three shells.
First strength experiment using a force from the top. The
strength of the shell was estimated by applying pressure to
the convex surface while the shell was resting on a balance.
The force at the break point was recorded. Each shell had a
specific noted state of infection and one could test for a
correlation. The force applied was in pounds per centimeter
squared.
First strength test with Cliona. A graph to show force
applied to shells versus the infection by Cliona celata. The
percent surface area bored by the Cliona celata is different
for each shell. Haliotis rufescens is used in this test, which
is described in Figure 3.
Figure 5
Figure 6
Figure 7
Figure 8
First strength test with Penitella. A graph to show force
applied to shells versus the infection by Penitella conradi.
nouber of hoes
The pereent surface area bored by the Penitella conradi is
different for each shell. Haliotis rufescens is used in
this test, which is described in Figure 3.
Second strength experiment using a force onto a strip of an
abalone. Because of the error involved in the first test,
the strength of the shell was estimated in this test by
cutting the shell into five or six one inch strips - the
middle one being used for the experiment. The measurements
were at first taken in pounds per square inch but the con¬
version was made to grams per cm2. Some of the strips were
not exactly an inch wide so an adjustment also had to be
made. The sequence of drawings shows the different steps
required in the experiment.
Second strength test. A graph to show the correlation be¬
tween the force applied onto the strip of shell and the
estimated overall percent of infection by Cliona celata.
Haliotis rufescens is used in this test, which is described
in Figure 6.
Second strength test. A graph to show the correlation between
the force applied onto the strip of shell and the estimated
overall percent of infection by Penitella conradi. Haliotis
rufescens is used in this test, which is described in Figure 6.
0
Figure 9
econd strength test versus density of shell. A graph to
show the correlation between the force required to break
the strip of shell and the density of the strip.
28
Jo

8
8

oo
Figure 1


6
2.


L
L

No

number of shells
2L


N
90 3

3
9
D
8
N
:
o
6
H
voo
Figure 2

I
E

number of shells




2
—


o
Figure 3
force
E
0



weights
abalone
balance
140
120
100
80
8 60
3 40
20

Figure 4
. . .


30 50 70 90
10
% surface area bored by clona
2

9
140
120
100
80
60
40
20
Figure 5
LP
2 4 6 8 10 12 4 16 18
no. of penitella per shell
Figure 6

8

abalone
is cut into strips
force

balance
fixed
350
300
250
200
8
2 10
8 100
50
0
Figure 7
0
0
0
0
E
10 30 50
70 90
% Surface area bored by clona
9
350
300
250
200
150
100
50
Figure 8
0
0
o 0

8 0
9 0
8
0

2 4 6 8 10 12 1 16 18
no. of penitella per shell
8
350
300
250
200
150
100
50
Figure 9
OXXROXOO
8
X 8 2
R
50 X0
X
R 0

10 12 14 16 18 20 22 24 25
density (gmem
of shell infected by cliona(x
penitella(o)