Download Parasites, density, and disturbance: Factors influencing coexistence

ABSTRACT
PARASITES, DENSITY, AND DISTURBANCE: FACTORS INFLUENCING
COEXISTENCE OF CERITHIDEA CALIFORNICA AND BATILLARIA
ATTRAMENTARIA
I investigated factors influencing coexistence of Cerithidea califomica and
Batillaria attramentaria in Bolinas Lagoon, California. Surveys conducted
throughout the lagoon (September 1994 and April 1996) evaluated habitat
utilization and species distribution. Field studies (July to October 1995)
evaluated parasite prevalence, susceptibility to parasitic infection, density
effects on growth and mortality, and response to substrate disturbance.
Cerithidea primarily occupied mud substrate, whereas Batillaria inhabited
diverse substrata. Over time Batillaria colonized new area; Cerithidea's
distribution remained unchanged. Cerithidea 15.00-20.99 mm had significantly
greater parasite prevalence (30%, SE = 9.09) compared to similar size Batillaria
(3%, SE
= 0.54); however, susceptibility was not significantly different.
Cerithidea had reduced growth rates in high density treatments and greater
overall per capita mortality. Early castration and sensitivity to increased
interaction may facilitate a density regulated displacement of Cerithidea by
Batillaria. In addition, Batillaria occupy all available substrates, leaving no
refuge for Cerithidea.
Sean Patrick McDermott
December 1996
PARASITES, DENSITY, AND DISTURBANCE: FACTORS INFLUENCING
COEXISTENCE OF CERITHIDEA CALIFORNICA AND BATILLARIA
ATTRAMENTARIA
by
Sean Patrick McDermott
A thesis
submitted in partial
fulfillment of the requirements for the degree of
Master of Science in Marine Sciences
in the School of Natural Sciences
California State University, Fresno
December 1996
TABLE OF CONTENTS
Page
LIST OF TABLES .
Vl
LIST OF FIGURES.
Vll
INTRODUCTION .
1
METHODS AND MATERIALS.
6
Study Site
.
6
Lagoon Survey .
8
Temporal Density Fluctuation
9
Response to Disturbance
11
Intraspecific Interaction
11
Prevalence and Susceptibility
15
RESULTS
18
Lagoon Survey .
18
Density Fluctuation
20
Colonization
23
Intraspecific Interaction
24
Parasitic Infection
30
DISCUSSION
.
38
LITERATURE CITED .
49
APPENDICES .
56
TEMPORAL DENSITY DATA
APRIL 1994 -AUGUST 1995
57
B.
COLONIZATION DATA .
61
C.
SIZE FREQUENCY DISTRIBUTION AND
DENSITY DATA .
66
A.
v
APPENDICES
Page
D.
SHELL GROWTH DATA
70
E.
LAGOON PARASITE PREVALENCE DATA .
78
F.
SOUTH MARSH STUDY SITE PARASITE
PREVALENCE DATA
81
INFECTING TREMATODE SPECIES DATA
88
G.
LIST OF TABLES
Page
Table
Habitat use by Cerithidea and Batillaria
in Bolinas Lagoon .
19
2.
Repeated measures ANOV A, colonization
24
3.
Two-way ANOV A, shell length change
27
4.
Two-way ANOV A, shell production .
27
5.
Two-way ANOV A, incidence of infection
37
1.
LIST OF FIGURES
Page
Figure
1.
Bolinas Lagoon, Marin County, California, U.S.A.
2.
Study site sampling stations, south marsh of Bolinas
Lagoon.
10
Dispersion of Cerithidea californica and Batillaria
attramentaria.
21
Temporal changes of Cerithidea and Batillaria
populations over 16 months.
22
Mean change in the ratio of Batillaria to Cerithidea
within two treatments of disturbance from 24
September 1995 through 21 October 1995 (21 days).
25
Growth of uninfected Cerithidea and Batillaria from
the south marsh of Bolinas Lagoon, 22 July 1995 to
30 September 1995.
28
Per capita mortality of Cerithidea and Batillaria in the
south marsh of Bolinas Lagoon, 22 July 1995 to 30
September 1995 .
29
Parasite prevalence with 95% C.I. for allopatric and
sympatric subpopulations throughout Bolinas Lagoon.
32
Parasite prevalence among eight, 2 mm size classes
of Cerithidea and Batillaria in the south marsh of
Bolinas Lagoon.
33
Percent of infections for the six most common trematode
species infecting Cerithidea and Batillaria for all size
classes in the south marsh of Bolinas Lagoon.
36
3.
4.
5.
6.
7.
8.
9.
10.
7
INTRODUCTION
Parasitic trematodes comprise an important part of soft sediment
marine communities (Blower and Roughgarden 1987, Sousa 1991, Rohde
1993). For example, they can influence the movement, migration, and
distribution of many intertidal gastropods (Lambert and Farley 1968,
Stambaugh and McDermott 1969, Holmes and Bethel1972, Kuris 1974,
Williams and Ellis 1975, Curtis 1987, 1990). Behavioral modifications are
considered a mechanism to facilitate transmission of the parasite to a second
intermediate host (Cannon 1979, Curtis 1990). Along the New England coast,
Ilyanassa obsoleta parasitized by the larval trematode Gynaecotyla adunca tend
to remain higher in the intertidal zone than uninfected individuals (Curtis
1990). This behavioral modification of I. obsoleta allows the release of the
parasite's cercariae stage near the second intermediate hosts, which include
the semi-terrestrial amphipods Talorchestia longicornis and T. megalopthalmia
and the fiddler crab Uca pugilator (Curtis 1990). Parasites have an impact on
many aspects of the host's population dynamics as well (Loker 1979, Kuris
and Warren 1980, May 1983, Sousa 1983, Brown et al. 1988, Lafferty 1993a,b,
Rohde 1981, 1993).
The primary effects of parasitic trematodes on marine molluscs include
complete castration of the adult (Kuris 1974, Baudoin 1975, Sousa 1983, Kabat
1986, Rohde 1993), reduced growth rates (Lafferty 1993a), increased mortality
(Sousa and Gleason 1989) and alteration of life history by delaying or
hastening maturity (Minchella 1985, Lafferty 1993b). At a high prevalence (the
percent of the population infected by parasites [Margolis et al. 1982]),
parasitic castrators can be density regulators of the host population (Lim and
2
Heyneman 1972, Kuris 1974, Combes 1982, May 1983, Lafferty 1993a).
Although the influence of parasites on intraspecific interactions has been
documented, the influence of parasites on community dynamics needs
further investigation (Sousa 1991).
The distribution of B. attramentaria overlaps the northern range of the
indigenous marine snail, Cerithidea californica. Cerithidea californica and
Batillaria attramentaria coexist in a few isolated populations within this
distribution overlap (Byers and McDermott, in prep.). Considered ecological
equivalents (MacDonald 1969) these two snails are closely related and utilize
the same habitat and resources. In addition, they are host to a similar
assemblage of parasitic trematodes (Emery 1979). The known existence of
persistent sympatric populations allows the evaluation of the interactions
between a native and recently introduced nonnative mud snail and the
examination of the influence parasitic castrators have on community
dynamics.
Batillaria attramentaria was first introduced to Tomales Bay, California
in the early 1930s and later to several bays ranging from Boundary Bay,
British Columbia to Moss Landing, California (Bonnot 1935, MacDonald 1967,
1969, Carlton 1992). Batillaria attramentaria does not have a pelagic larval stage
(Yamada and Sankurathri 1977). Incidental introductions related to the
commercial oyster Crassostrea gigas was the primary mechanism for
colonizing various geographic locations (Bonnot 1935). Crassostrea gigas were
planted in Bolinas Lagoon from 1955 to 1956 (B. Johnson, pers. comm.). Initial
introductions of B. attramentaria into Bolinas Lagoon most likely occurred
during this time. Sympatric populations of C. californica and B. attramentaria,
previously documented exclusively in Millerton Marsh, Tomales Bay
3
(Driscoll 1972, Whitlatch 1974, Emery 1979, Whitlatch and Obrebski 1980),
now occur in Bolinas Lagoon, California.
Direct comparisons of these two snail species include an analysis of the
feeding structure morphology (Driscoll 1972) and one field study evaluating
the effects of interspecific interaction (Whitlatch and Obrebski 1980).
Independent assessment of life history and physiological tolerance indicate
several shared ecological characteristics. These studies indicate that both
snail species are long-lived, iteroparous organisms; individuals live
approximately 10 years and are reproductively mature after 2 years
(Whitlatch 1974, Race 1981). Females deposit egg strings from late spring to
early summer and hatch as crawling juveniles (MacDonald 1967; Yamada and
Sankurathri 1977; McCloy 1979; Race 1981). Diatoms constitute the main diet
for both snail species (Whitlatch 1974, McCloy 1979, Whitlatch and Obrebski
1980). However, C. californica is better adapted to feeding on fine grain
organic material (Driscoll 1972). Cerithidea californica has a high tolerance to
salinity and temperature changes and the ability to survive long periods of
desiccation (Race 1981); juvenile B. attramentaria are highly susceptible to
desiccation (Whitlatch 1974). Dispersal is presumably accomplished by the
adult but juveniles, and adults, can float on the water surface by expansion of
their foot (MacDonald 1967; Whitlatch 1974; Whitlatch and Obrebski 1980,
Race 1981). Adult B. attramentaria crawl longer distances over a given period
than C. californica (Whitlatch 1974, Whitlatch and Obrebski 1980). Shore birds
(Sousa 1993) and rafting (Race 1981, McDermott, pers. obs.)- the snails attach
to drift Ulva sp. or debris- can enhance dispersal. Shore birds, such as
Willets (Catoptrophorus semipalmatus) prey on small C. californica. Some snails,
however, are expelled alive in new locations.
4
At least 20 species of parasitic trematodes infect C. californica (Martin
1955, 1972), permanently castrating the host (Sousa 1983). Batillaria
attramentaria is host to the same assemblage of parasitic trematodes that
castrate C. californica (Emery 1979). The effects of parasitic trematode infection
on C. californica include selecting for early maturation in areas of high
prevalence (Lafferty 1993b ), decreased reproductive output, reduced growth
rates, and increased mortality (Sousa 1983, Sousa and Gleason 1989, Lafferty
1993a); similar studies have not been conducted for B. attramentaria.
Differential parasite prevalence and susceptibility to parasitic infection
could have significant repercussions on the community dynamics. A greater
incidence of infection within the first years of reproductive capability could
reduce the reproductive output of that species early in its life history. In
addition, castration in younger size classes could increase mortality for that
year class (Sousa 1983). As a nonnative species, B. attramentaria may be less
susceptible to infection by parasites common to the California coast. The
potentially reduced susceptibility to parasitic infection, therefore a lower
incidence of infection, may affect the reproductive output of B. attramentaria
compared with C. californica.
Previous field studies indicated coexistence of the two snail species
(Whitlatch and Obrebski 1980); however, new field observations that I have
made suggest displacement of C. californica from sympatric sites. This study
was undertaken to investigate factors potentially mediating the interaction
between C. californica and B. attramentaria. The questions addressed were:
1. Do the snails utilize similar microhabitats within Bolinas Lagoon?
2. Do C. californica and B. attramentaria respond similarly to substrate
disturbance and availability?
5
3. How does intraspecific interaction affect the growth rate, mortality
and reproductive output of C. californica and B. attramentaria and how are
these factors affected by parasitic castration?
4. In sympatric subpopulations, does a differential parasite prevalence
exist between C. californica and B. attramentaria?
5. Are C. californica and B. attramentaria equally susceptible to parasitic
infection?
6. How does parasite prevalence within sympatric subpopulations
compare with allopatric subpopulations?
METHODS AND MATERIALS
Study Site
Bolinas Lagoon is an intertidal estuary located 25 km northwest of San
Francisco, California (Figure 1) and is one of few places where populations of
Cerithidea californica and Batillaria attramentaria coexist in approximately equal
densities (Byers, in prep., McDermott, pers. obs.). Sympatric and allopatric
subpopulations are scattered along the eastern bank with the largest
sympatric subpopulation located in a marsh ("south marsh") at the lagoon's
southeastern-most point. The south marsh is a 10- hectare intertidal marsh
system that has been expanding as a result of anthropogenic activity. The
Eskoot Creek and other tidal creeks wind through the center of the marsh,
emptying into Bolinas Lagoon. During the winter rainy season, the creek is a
source of fresh water, silt, and debris. A causeway, formerly at the marsh
front, blocked direct tidal action and slowed drainage of the creek for over 40
years. Consequently, sediment accumulation transformed a rich intertidal
mudflat habitat into a well-developed marsh system (pers. comm. John
O'Connor, 1995). Removal of the causeway and an adjacent landfill from the
lagoon in November 1993 opened the marsh system to a natural tidal flux,
reversing the sedimentation state from depositional to erosional. Cerithidea
californica and B. attramentaria occur throughout the south
marsh: in the tidal creeks, on the mudflats, and in the vegetation up to
approximately +1.07 m above Mean Lower Low Water (MLLW). Both snail
species are most abundant within shallow depressions on the open mudflats.
7
Pacific
Ocean
Lagoon
0
10
20 km
Figure 1. Bolinas Lagoon, Marin County, California, U.S.A.
8
These depressions, or pans, vary in size (<15m2 to >280m2) and elevation.
Most remain wet, but not submerged, during ebb tide. Tides greater than
+1.04 above MLLW overflow all pans. Vegetation is rare within pans.
Salicornia virginica, Distichlis spicata, Jaumea sp., and Spartina foliosa constitute
the dominant marsh flora.
Many infaunal species inhabit the tidal channels and mudflats within
the lagoon's south marsh. Mudflats and pans provide habitat for an array of
infauna including the gammarid Corophium sp., the polychaete Exogone lourei,
and the introduced bivalve Gemma gemma. The most distinct infaunal species
is the decapod Callianassa sp., the ghost shrimp. Callianassa sp. burrow into
the sediment, creating tunnels to dwell in. The excavated sediment produced
by the burrowing activity forms mounds scattered about the inhabited
mudflat. Several mounds can be attributed to a single adult. This activity
alters the surface sediment structure. Well- sorted, silty mud, habitat
commonly inhabited by C. californica, becomes an area of fine grain sand. The
expansion of Callianassa sp. populations on Kent Island, located at the western
bank of Bolinas Lagoon, altered the substrate on which a localized population
of C. californica occurred. The burrowing activity of Callianassa sp., and the
subsequent habitat modification, was responsible for a localized extinction of
C. californica on Kent Island (Sousa 1993). Although not abundant, the number
of Callianassa sp. mounds in the south marsh noticeably increased between
1994 and 1995.
Lagoon Survey
A survey of Bolinas Lagoon conducted on 12 September 1994 at low
tide evaluated habitat use and general distribution of C. californica and B.
attramentaria. A visual inspection of the intertidal zone included the
9
perimeter of Bolinas Lagoon, the Pine Gulch Creek delta and the south marsh.
I noted snail species, vegetation, and substrate type when any one factor
changed. Snail densities were evaluated using haphazardly placed 23x23 ern
square quadrats (529 crn2). The lagoon was re-surveyed on 14 April1996 to
evaluate changes in the distribution of C. californica and B. attramentaria that
had occurred in the 18 month period. An additional survey of species
composition and distribution in Tomales Bay (Byers and McDermott, in
prep.) allowed for a comparison of the short-term changes in Bolinas Lagoon
with changes in Tomales Bay since the late 1970s.
Temporal Density Fluctuation
If B. attramentaria are indeed displacing C. californica, the abundance of
C. californica would decrease with increasing B. attramentaria abundance. I
monitored the south marsh population to document density fluctuation of C.
californica and B. attramentaria, separately and combined, between
reproductive seasons. Sampling was conducted as follows.
Four marsh pans (stations 1, 2, 4, and 5 on Figure 2), hereafter called
'stations', were selected for monitoring based on accessibility with minimal
disturbance; stable substrate bordering a pan was required to provide a work
area. Wood planks used to access sampling stations minimized impact of
sampling activity on the mudflats. I estimated population densities at each
station by averaging the number of snails of each species, >10 rnrn in length, in
the top 1 ern of sediment, from 6 subsarnple quadrats (529 crn2). Mean density
per sampling date was the average of the four stations (n = 4). Sampling was
conducted in April, September, October 1994 and February,
10
Marsh channels
and open mudflat
f./:·::-::::-::-::J Marsh Vegetation
Upland vegetation
Figure 2. Study site sampling stations, south marsh of Bolinas Lagoon.
11
May, August 1995. Independent t-tests were used to evaluate the change in
species and total density between successive reproductive seasons.
Response to Disturbance
The south marsh has long been a sedimentary environment. Recent
changes have altered the hydrodynamics and created an erosional setting.
Channels are deepening (McDermott, unpublished data 1994) and the flora
composition adjacent to several marsh pan stations has changed (McDermott,
pers. obs.). In addition, field observations have noted large patches of B.
attramentaria in areas disturbed by dredging. I evaluated the differential
response to disturbance using substrate manipulation treatment plots. Three
1 m2 plots were marked with wooden stakes. One remained undisturbed as
the control for snail presence and ambient conditions. The second treatment
had surface snails removed (species noted and counted) to test the response to
available substrate. The third treatment tested for a response to disturbance
by removing all snails and the top 3-4 em of sediment. Plots were replicated
at three stations (n
= 3)- stations 1 through 3 (Figure 2).
Each plot was
subsampled weekly for 28 days by counting the number of each snail species
within six 20x20 em square quadrats. Averaging weekly subsamples provided
a single density value for each treatment. Snail density data were converted
to the ratio of B. attramentaria to C. californica (B:C ratios) for analysis with
repeated measures analysis of variance (ANOVA).
Intraspecific Interaction
Increased intraspecific interaction, by increasing density, negatively
affects the life history of Cerithidea californica (McCloy 1979, Lafferty 1993a).
Under such conditions, mortality increases and growth rates decrease. As a
12
potential method to limit interaction, C. californica displayed greater outward
migration from areas of artificially increased density (McCloy 1979). Field
work has not been conducted to evaluate the effects of increased density, and
intraspecific interaction, on the life history of B. attramentaria. Therefore, I
conducted a field study to evaluate the effects of intraspecific interaction on B.
attramentaria. Cerithidea californica were subjected to the same evaluation
for a direct comparison. Field experiments are currently in progress
evaluating the effects of interspecific interaction at varying density levels (J.
Byers, pers. comm.).
I scanned the south marsh to locate accessible pans greater than 14m x
3 m and inhabited by both species. Seven pans were selected as stations
(Figure 2). I estimated the size frequency distribution and population density
for each species using ten 612 cm2 circular quadrats haphazardly placed at
each station. The species, number, and size of all snails between 15.00 and
30.99 mm, from apex to siphonal canal, on the substrate surface and within
the quadrat were recorded. Multiplying the estimated station density by the
frequency of individuals from eight 2.0 mm size classes established the
percent size frequency distribution for each species. Densities and size
distributions were not standardized among stations; experimental
populations within treatments were based on ambient population dynamics
at each station to minimize confounding factors. I did not transplant snails
among stations. It is not clear whether individuals of both species migrate
among pans, therefore mixing of subpopulations was minimized to maintain
potential genetic integrity among pans.
Experimental manipulations of density consisted of five treatments as
follows: (a) the mean density of C. californica and B. attramentaria combined,
13
(b) mean density of C. californica with B. attramentaria removed and replaced
by an equal number of C. californica, (c) mean density of C. californica with B.
attramentaria removed without replacement, (d) mean density of B.
attramentaria with C. californica removed and replaced by an equal number of
B. attramentaria, and (e) mean density of B. attramentaria with C. californica
removed without replacement. Treatment (a) acted as a control for ambient
density and interspecific interaction. Treatments (b) and (d) evaluated the
effect of intraspecific interaction at densities similar to those with interspecific
interaction, while treatments (c) and (e) assessed the effects of intraspecific
interaction. with densities lowered by the removal of one species. As a control
for cage effects on growth, approximately 70 measured (±0.5 mm) and labeled
individuals of both species were released at each station.
To collect the number of snails needed from each station for the
experimental populations, I scraped the surface layer of sediment into a 1 mm
mesh sieve and rinsed with sea water. Retained snails were washed with fresh
water and separated by species, station, and 2.0 mm size class. Restricted
growth estimates to one size group (hence, age class) reduced confounding
factors associated with differential growth rates due to allometry (Race 1981,
Sousa 1983, Lafferty 1993a). Growth was evaluate in the target size group of
21.00 - 24.99 mm. These individuals were measured (±0.5 mm) from the tip of
the apex to the siphonal canal (length) and labeled with numeric paper wire
markers attached to the dorsal side of the shell with Krazy@ glue. In addition,
I marked the lip of the shell at the mantle edge with a Sharpie@ marker to
estimate relative shell growth rates measured as shell production. Disparate
mechanisms of shell production and erosion could compromise the
significance of comparing shell growth measured as the change in shell length
14
from the apex to the siphonal canal. This alternate technique to evaluate
growth, by measuring shell production at the mantle edge, permitted a
comparison between methods for sensitivity to detect growth and to assess the
relationship between shell length change and shell production. The
remaining individuals were distinctly tagged by size class with Sharpie@ or
Testors@ enamel paint. Once labeled and tagged, I assigned individuals to
experimental populations according to treatment.
Circular enclosures (612 cm2) were constructed of 0.08 inch thick clear
polypropylene Naltex® mesh (1.0 mm opening) secured with cable ties.
Covers were not used to reduce possible shading effects. Consequently,
snails could escape with flood tides greater than +1.65 m above MLL W. I
placed the enclosures along the midline of the mudflat. Enclosures extended
61 em above and 10 em below the sediment surface. Placement of enclosures
disturbed considerably the sediments within the enclosed area. The
experiment started eight days after enclosures were in place, allowing
sediments and diatoms to equilibrate near ambient conditions. Experimental
populations were randomly placed into enclosures on 22 July 1995, seven
days after the initial snail collection.
I monitored experimental populations twice per month from July to
September 1995 for missing and dead individuals; mortality within the target
size classes was recorded. Missing and dead snails were replaced by
individuals from similar size classes. If a labeled snail from the target size
classes escaped or died, another individual of approximately the same size
replaced it; replacement snails were not used in the data analysis. I collected
all snails on 30 September 1995 for the final growth measurements. All live
snails were dissected for determination of parasitic infection. For each
15
treatment, the average change in shell length and the average shell production
for individuals initially 21.00 to 24.99 mm provided a growth estimate for that
site (n
= 7).
Egg strings were not found; therefore, reproductive output could
not be evaluated. The effects of density on growth, measured in shell length
and shell production, for nonparasitized snails were analyzed independently
using model 1, 2-way ANOVA. Mortality was calculated as per capita
mortality and investigated using chi-square analysis (X2) to assess the
relationship of density treatments and survivorship. A heterogeneity chisquare was conducted to evaluate homogeneity of the treatments to
determine if pooling the data was justified.
The significance level established, to reject the null hypothesis of no
difference, for all statistical analyses wasp
= 0.05.
I tested homogeneity of
variances prior to all statistical tests using an F-test or Cochran's method as
required.
Prevalence and Susceptibility
I evaluated parasite prevalence at allopatric C. californica and B.
attramentaria subpopulations and from sympatric subpopulations
throughout Bolinas Lagoon. Snails from 20-25 mm were collected during the
September 1994 lagoon survey and dissected for positive determination of
parasitic infection. Prevalence throughout the lagoon was not sampled
temporally. I conducted a x2 to evaluate the relationship between snail
species prevalence, separately, and subpopulation (allopatric and sympatric).
Confidence intervals (95% C.I.) were calculated. Cochran's method for
continuity correction was routinely employed for all chi-square analyses (Zar
1984).
16
Further evaluation of parasite prevalence and incidence of infection
within a subpopulation of coexisting C. californica and B. attramentaria was
conducted as follows. I collected Cerithidea californica and B. attramentaria
15.00 mm to 30.99 mm from the south marsh during July and September 1995.
Snails were separated by species into eight 2.0 mm size classes and dissected
for positive determination of parasitic infection. Parasites were identified to
lowest possible taxon (Martin 1972). Combining prevalence data from both
collection dates and for all size classes provided an estimate of overall
parasite prevalence, with 95% C.L calculated, for both snail species. Chisquare analysis was used to test the relationship between parasite prevalence
and snail species.
I evaluated the relative susceptibility to parasitic infection using
uninfected snails from two size classes. Snails 16.00-17.99 mm were collected
(from stations 1, 2, 3, and 4; Figure 2) and grouped into compartmentalized
containers by species, three per cell, with sea water and placed under
incandescent light for 32-40 hours. This process induces shedding the
cercaria! stage of the parasites (Lafferty 1991). I evaluated the effectiveness of
the shedding technique by repeating the process and dissecting non-shedding
individuals for positive determination of parasite absence. Individuals from
cells with free-swimming cercariae present were considered infected and not
used. I randomly selected 70 cells (210 individuals) of non- shedding snails
for each species. At each of the eight stations, 30 C. californica and 30 B.
attramentaria were placed into separate mesh enclosures, constructed as
described above. Snails remained in the field, exposed to ambient levels of
free swimming trematode miracidia or to trematode eggs for 28 days (21 July19 August). I transferred all recovered snails from each station directly to
17
containers, by station. Snails were maintained in the lab with running sea
water. After 31 days, I dissected live snails for positive determination of
parasite infection. Parasites were identified to lowest possible taxon. Snails
21.00-22.99 mm underwent the same treatment; this size class remained in the
field 35 days (28 August through 1 October 1995) and in the lab for 30 days.
Differential susceptibility of snails to parasitic infection was investigated with
a model 1, 2-way ANOV A.
RESULTS
Lagoon Survey
Cerithidea califomica and B. attramentaria inhabited all suitable
microhabitats. Distribution was generally limited by elevation; areas that
remained dry at most high tides, denoted by the presence of the salt marsh
grass, D. spicata, and Jaumea sp., or continuously immersed below MLLW
were not inhabited by either snail. Spatial separation was not apparent within
sympatric subpopulations. Batillaria attramentaria was observed to inhabit
areas of all substrate types including cobble and rock (Table 1). Ceritlzidea
californica primarily occurred on silty mud substrates and rarely inhabited
areas of sand substrate, even though sand substrate was frequently adjacent to
inhabited mudflats.
Isolated allopatric subpopulations continue to persist in the lagoon,
such as the C. californica subpopulation on the Pine Gulch Creek Delta, the
largest and most isolated allopatric subpopulation. The largest
subpopulation of B. attramentaria, spatially, occupied a 0.6 km length of
shore, the substrate consisting of sand, small rock, and cobble. Densities of B.
attramentaria in this area ranged from 180 to 1900/m2. Allopatric
subpopulations of B. attramentaria inhabiting low energy mudflats had the
highest snail densities. Estimates up to 4700 B. attramentaria per m2 were
calculated on a mudflat adjacent to the south marsh; density estimates for C.
californica varied little among microhabitats and with interspecific interaction.
Temporal changes in snail species distribution throughout Bolinas Lagoon
indicated a stable, though patchy, subpopulation structure of C. californica
19
Table 1. Habitat use by Cerithidea and Batillaria in Bolinas Lagoon.
Habitat Features
Low salinity*
Cerithidea
Batillaria
--.)
--.)
Low intertidal**
t
Marsh pans
--.)
Substrate type
Mud
--.)
--.)
Sand
t
--.)
Gravel
--.)
Rock
--.)
Vegetation
Distich! is
--.)
--.)
Salicornia
--.)
--.)
Spartina
--.)
--.)
no vegetation
--.)
--.)
* 10-15 ppt
** areas exposed at < 0.0 m MLLW
t rare
20
and dynamic B. attramentaria subpopulations. Variation of C. californica
distribution may be an attribute of low densities estimated within these
specific areas (Figure 3). For example, allopatric subpopulations of both snail
species at the lagoon's northern point noted in the April 1996 were not
observed during the initial survey. Qualitative estimates of density within
these areas indicated <1.0 snail per m2. On the other hand, B. attramentaria
had significant changes in the distribution along the southern sandspit bank
of the lagoon (Figure 3). The habitat along this bank is primarily sand
substrate with vegetation (Distichlis spicata) limited to the upper tidal zone.
Few or no C. californica occupied this area whereas B. attramentaria were
common.
Density Fluctuation
A seasonal fluctuation of snail density occurred as expected; the trend
in fluctuation for C. californica, however, was not anticipated. Ceritlzidea
californica had a noticeable yet slight winter decrease in surface dwelling
snails. More significantly, the number of C. californica did not return to prewinter levels during in either the May 1995 or August 1995 surveys.
Conversely, B. attramentaria had a distinct decrease in surface dwelling snails
during February 1995 followed by a sharp increase in May and August 1995
(Figure 4). The combined mean density (C. californica +B. attramentaria)
fluctuated between April, September, and October 1994. The expected winter
drop in the combined density occurred in February 1995 and remained
slightly reduced through May and August 1995, compared to pre-winter
estimates.
21
O.Okm
September 1994
l%/~1 Cerithidea
m
Batillaria
Sympatric
subpopula tions
Bolinas
Lagoon
Bolinas
Bolinas Bay
April1996
Bolinas
Lagoon
N
t
Bolinas Bay
Figure 3. Dispersion of Cerithidea and Batillaria in Bolinas Lagoon, California. PGCD
Gulch Creek Delta.
= Pine
22
Cerithidea
D
Apr 94
Sept 94
Oct 94
Feb 95
May 95
Batillaria
Aug 95
Sampling Month
Figure 4. Temporal changes of C er it hide a and Bat ill aria populations over
16 months. Sampling was conducted in he south marsh of Bolinas Lagoon.
Means per 23 x 23 em quadrat with SE; n = 4.
23
Evidence for displacement of C. californica was indicated in the yearly
return of adults and 2nd year individuals between reproductive seasons. The
mean density of C. californica (> 15.0 mm) decreased significantly (p = 0.031)
from April 1994 (22.58/529 cm2, SE = 3.83) to August 1995 (12.04/529 cm2, SE
= 2.59). An increase in the mean density of B. attramentaria was evident
between April1994 (14.38/529 cm2, SE = 3.56) and August 1995 (19.71/529
cm2, SE = 3.91), although the increase was insignificant (p = 0.176). The
decrease in the mean combined species density between April1994 (37.00/529
cm2, SE = 5.81) and August 1995 (31.75/529 cm2, SE = 5.22) was also
insignificant (p= 0.2633). The statistical significance reflected the biological
trend with the mean density of C. californica decreasing in conjunction with
slight increases of B. attramentaria densities, indicating short-term changes of
the community dynamics in the direction of lower C. californica abundance
and greater B. attramentaria abundance.
Colonization
Significant results from the colonization study supported field
observations of elevated B. attramentaria abundance within disturbed patches.
Substrate manipulations indicated no significant response of the species ratio
to disturbance levels; however, a differential response to disturbance over
time was evident (Table 2). The Batillaria: Cerithidea ratio (B:C ratio) for the
high - impact (cleared) and low - impact (picked) treatments increased over
the first 2 weeks, remaining greater than the undisturbed controls for the first
3 weeks (Figure 5). Ratio estimates for weeks 3 and 4 were less than the peak
after 2 weeks, indicating a slow colonizing of C. californica into the
manipulation plots with possible emigration of B. attramentaria. The B:C ratio
for the lightly impacted treatment approximated an ambient value during the
24
4th week while the high impact treatment estimates were consistently greater
than ambient estimates. Control plots demonstrated natural fluctuation of
snails within the study site, however, the B:C ratio within control plots varied
little over the 4 - week period compared to the manipulated plots. The
observed trends and statistical data demonstrate a greater initial colonizing
ability by B. attramentaria into newly available substrate compared with C.
californica.
Table 2. Repeated measures ANOV A, colonization. Colonization of
Cerithidea and Batillaria into 3 substrate disturbance treatments over 4 weeks.
SS = sum of squares, MS = mean square. * = significantly different.
df
Source
Treatment
2
Subject
(Group)
5
Time
4
Timex
Treatment
8
Time x Subject
(Group)
20
ss
92.874
MS
46.437
F- Value
1.445
P- Value
0.3196
160.657
330.061
32.131
82.515
6.146
0.002 *
154.155
19.269
1.435
0.2424
268.519
13.426
Intraspecific Interaction
The two methods used to evaluate growth had similar results for
uninfected snails. The magnitude of growth detected differed between
methods for evaluating growth rates, resulting in a distinct difference in the
sensitivity between methods. Measuring the change in shell length over time
as an indication of growth did not reveal a significant effect of species
interaction or of density (Table 3). The change in shell length for C.
25
Control
~
~
Picked
Cleared
18
16
14
lil 12
':5
~ 10
~
........
.:=... 8
~
~
t:Q
6
4
2
0
0
1
2
3
4
Week
Figure 5. Mean change in the ratio of Batillaria to Cerithidea within two
treatments of disturbance from 24 September 1995 thru 21 October 1995 (27d).
The cleared treatment had the top 2 em of surface sediment removed while the
picked treatment had only surface snails removed. n=3; error bars = SE.
26
= 0.169); however, was significantly less than for B.
attramentaria (1.74 mm, SE = 0.299). Conversely, an analysis of variance
californica (0.902 mm, SE
comparing growth measured by shell production, in uninfected snails,
indicated significant interaction between density treatment and snail species
(Table 4). A Bonferroni pairwise comparison for all six possible comparisons
(treatment x species) indicated significantly less shell production in C.
californica from the high- density treatment than for B. attramentaria from high
(p
= 0.008) and low (p = 0.05) density treatments (Figure 6).
Shell
production in C. californica was greater, though not significantly (p
= 0.136),
from the low - density treatment than the high - density treatment. Data
collected for shell production in treatment A, effects of species interaction,
were not used in this analysis because the sample size was inadequate for
equal replication among treatments.
A regression analysis of shell production against shell length change
indicated a weak correlation between these two methods of estimating growth
rates. Cerithidea californica's correlation coefficient (r2
= 0.577, df = 1, p < 0.05)
was slightly less than for B. attramentaria (r2 = 0.603, df = 1, p < 0.05). The
regression equation for C. californica was
Yi
= 2.258 + 3.319(Xi)
(1)
= 2.949 + 3.146(Xi)
(2)
and for B. attramentaria,
Yi
Shell production may be a more sensitive method for evaluating
environmental impacts on growth for these snail species.
Mortality was consistently greater for C. californica than B. attramentaria
(Figure 7). The heterogeneity chi-square indicated treatments were not
homogeneous, therefore the data were not pooled among treatments.
27
Table 3. Two-way ANOV A, shell length change. Comparison of growth
rates, measured as shell length, between Cerithidea and Batillaria from high
and low density treatments. SS = sum of squares, MS = mean square. * =
significantly different.
Source
Treatment
Species
Treatment
x Species
Residual
ss
4.497
MS
0.045
4.497
F- Value
0.041
4.156
P- Value
0.9886
0.0498 *
1
3.145
3.145
2.907
0.0979
32
34.624
1.082
df
3
1
0.134
Table 4. Two-way ANOVA, shell production. Comparison of shell growth
rates, measured as shell production, between Cerithidea and Batillaria from
high and low density treatments. SS = sum of squares, MS = mean square. * =
significantly different.
Source
Treatment
Species
Treatment
x Species
Residual
ss
8.346
MS
67.291
8.346
F- Value
9.008
1.117
P- Value
0.0095 *
0.3084
1
49.147
49.147
6.579
0.0225 *
14
104.584
7.470
df
1
1
67.291
28
Cerithidea
Batillaria
12
4
10
-=
E 8
E
+
4
Low
High
5
t
0
;;:;::
u
='
6
"'"'
Qj
4
"0
e
..!:
5
tJJ
2
~
0
High
Ceritlzidea
Low
Batillaria
Density Treatment
Figure 6. Growth of uninfected Cerithidea and Batillaria from the south
marsh of Bolinas Lagoon, 22 July 1995 to 30 September 1995. Mean growth
rate with SE. Values above bars are sample size.
29
D
High density
~ Cerithidea
Low density
~ Batillaria
20
18
-
16
(41)
~ 14
~
~ 12
.....1-<
0
~
10
.....fll
'5.. 8
!11
u
1-<
ClJ
6
P...
4
(31)
(31)
0
0
2
0
High
Low
Cerithidea
High
Low
Batillaria
c
B
Interaction
Density Treatment
Figure 7. Per capita mortality of Cerithidea and Batillaria in the
south marsh of Bolinas Lagoon, 22 July 1995 to 30 September 1995. High
and Low represent the density treatments. Interaction represents the
control for ambient density and interaction. Values above bars are
sample size.
30
Treatments were analyzed independently with
x2 analysis.
Mortality of C.
californica was significantly greater than in B. attramentaria at ambient
interaction and density levels (treatment A) and for high intraspecific
densities (treatment B). Low intraspecific interaction resulted in the least
mortality of C. californica (Figure 7) which was greater than, though
not significantly, mortality of B. attramentaria from the low intraspecific
interaction treatment (E). It is not known whether the snails were infected
with parasitic trematodes prior to placement in the field, thus the influence of
parasites on mortality rates cannot be assessed.
Cage construction was successful in retaining snails. However, the
highest flood tides exceeded the height of the enclosure. Snails crawled up
the enclosure wall or floated as the tide came in. Recovery of labeled snails
varied among stations from 42% to 86%.
Parasitic Infection
Parasite prevalence varied among sites throughout the lagoon.
Batillaria attramentaria from a sympatric location approximately 0.4 km north
of the study site had the greatest percent infection, 89%, while C. californica
from an isolated sympatric location along the marsh front, in the south marsh,
had the least prevalence, 0.0%. Chi-square analysis indicated a trend of
greater parasite prevalence in snails from sympatric subpopulations as
compared to snails, of the same species, from allopatric subpopulations
(Figure 8). No significant difference was indicated between allopatric C.
californica subpopulations compared with allopatric B. attramentaria
subpopulations. Chi-square analysis indicated significantly lower parasite
prevalence for C. californica coexisting with B. attramentaria (Figure 8). This
finding is contradictory to parasite prevalence data from a sympatric
31
subpopulation site discussed later. Sample sizes were small and limited to
individuals 20.00 to 25.00 mm long. Better characterization of prevalence
among subpopulations throughout the lagoon requires further sampling of
more snails from a variety of size classes.
Chi-square analysis indicated overall estimated parasite prevalence for
= 18.44 - 22.55) was significantly greater (p < 0.05)
attramentaria (14%, 95 % C.I. = 13.29- 14.94) over the duration of the
C. californica (22%, 95 % C.I.
than B.
field study. Examination of parasite prevalence after subdividing the
population into 2.0 mm size classes revealed unexpected results (Figure 9).
Smaller C. californica (15.00 to 20.99 mm) were more frequently infected than
similar size B. attramentaria; conversely, larger C. californica (27.00 to 30.99 mm)
were less frequently infected than similar size B. attramentaria. The 2.0 mm
size classes were further combined into three groups: 15.00- 20.99 mm, 21.0026.99 mm, and 27.00 - 30.99 mm. A heterogeneity chi-square analysis of the
contingency tables for prevalence between species for the three size groups
indicated the data were not homogeneous, further indicating a significant
relationship between snail species, size class, and parasite prevalence.
Independent
x2 tests by size group were conducted.
from the 15.00 -20.99 mm size class (30%, 95% C.I.
Cerithidea californica
= 15.98- 32.24) had a
significantly greater percent infection (p < 0.05) then observed for B.
attramentaria (3%, 95% C.I.
= 1.67- 4.82) from the same size range.
Conversely,
the estimated percent infection for C. californica from the 27.00- 30.99 mm size
group (32%, 95% C.I.
= 22.45 - 33.49) was significantly less (p < 0.05) then
similar size B. attramentaria (56%, 95% C.I.
= 55.99 - 71.28).
Estimated percent
infection for the size group 21.00 to 26.99 mm was not significantly
32
Ill Allopatric
•
Sympatric
70
137
60
-
50
Q.l
40
~
0
._
u
c::Q.l
ttl
>
Q.l
122
70
30
93
1-<
p,.,
20
10
0
t
Allopatric
Sympatric
Cerithidea
Allopatric
Sympatric
Batillaria
Figure 8. Parasite prevalence with 95% C.I. for allopatric and sympatric
subpopulations throughout Bolinas lagoon. Snails were collected 12 Sept
1994. Number of snails examined from each subpopulation is given.
33
Cerithidea
D
Batillaria
90
80
70
c:0
~
-.£
c:
60
50
u
~
..
"iii 40
«<
«<
t:l..
~
0
30
20
10
0
~
..0
.....
I
.....
II')
~
oci
.....
r-!..
......
~
~
- ~
I
0'\
~
N
~
~
I
~
~
~
~
~
co
N
~
~
~
0'\
N
Size Class (mm)
Figure 9. Parasite prevalence among eight, 2 mm size classes in the
south marsh of Bolinas Lagoon. Prevalence calculated from July and
September 1995 data combined. Snails were collected from the seven
designated sampling stations. Error bars are the upper 95% C.I.
34
different (p > 0.05) between species (C. californica = 19%, 95% C.I. = 0.1619.01; B. attramentaria = 15%, 95% C.I. = 0.15- 18.26).
Five of the seven stations monitored for prevalence had approximately
equal densities of C. californica to B. attramentaria. The remaining two stations
had greater densities of B. attramentaria. A post-hoc investigation of parasite
prevalence was conducted based on relative equality of species density.
Prevalence in C. californica (17%, 95% C.I. = 15.01 - 17.38) was significantly
greater than for B. attramentaria (13%, 95% C.I.
= 11.39- 13.77) from the five
stations in which snail density was approximately equal. At the two stations
with lower densities of C. californica than B. attramentaria; parasite prevalence
was greater for C. californica (30%, 95% C.I.
attramentaria (17%, 95% C.I.
= 25.12- 36.61) than for B.
= 14.16- 21.02).
These data indicate a differential
prevalence between snails independent of density.
Six species of parasites comprised 76% of all infections within the south
marsh. A similar assemblage of trematodes infected Cerithidea californica and
B. attramentaria. The most prevalent trematode species, however, was not the
same for both snails (Figure 10). Parorchis acanthus was the most common
trematode in C. californica, identified in 60% (95% C.I.
= 49.97- 67.96) of
infected individuals. Euhaplorchis californiensis was the most common
trematode species in B. attramentaria, accountable for 45% (95% C.I.
= 35.78-
55.07) of infected individuals. Size of the snail did not affect the common
trematode species or the parasite assemblage between snail species. Other
trematode species, each constituting a small percentage of infections,
remained unidentified. Combined, these unidentified trematode species
comprise a substantial component of the trematode assemblage. Double
infections were noted in only five individuals.
35
Although parasite prevalence varied among size classes and between
species, differential susceptibility was not distinguished between C. californica
and B. attramentaria. No significant difference in susceptibility was detected
between snail species or size class (Table 5). Cerithidea californica and B.
attramentaria 16.00 - 17.99 mm had similar incidence of infection, 11.4% (95%
C.I. = 7.6- 18.6) and 11.1% (95% C.I. = 5.4- 14.9), respectively. Incidence of
infection was only slightly greater for C. californica (9.1 %, 95% C.I. = 4.5- 14.7)
from the 21.00- 22.99 mm size class compared with similar sized B.
attramentaria (5.3%, 95% C.I.
= 3.5 - 12.9).
An evaluation of the shedding
method used to discriminate uninfected and infected snails indicated an 89%
to 92% effectiveness relative to positive evaluation techniques (e.g.,
dissection). Therefore, error in the initial evaluation for infection may be
responsible for a significant portion of new infections noted.
Snail size and maturity were not quantitatively correlated prior to this
study. Maturity was noted, based on presence or absence of gonadal material,
during dissection at the end of the susceptibility study. Presence of gonadal
material does not reasonably imply reproductive maturity, but does provide a
nutrient source for trematodes. These data suggest C. californica mature at a
smaller shell size compared with B. attramentaria. From the 16.00- 17.99 mm
size class, 5.5 % (n
(n
= 207) of B.
fully mature.
= 162) C.
californica were immature compared with 16.43 %
attramentaria. All individuals from the 21.00- 22.99 mm were
36
Cerithidea
(n = 132)
D
Batillaria
(n = 106)
80
70
60
~
..g
50
1.1
]
40
~
30
.....0
"
20
10
0
.s
.§
E
c.:::
.!!)
-E
~
~
:::!
~
"'
E
~
:a
o"'
.!!)
..::
l:
\:
~
~
"':::!c
:s
!"'
-~
t!
~
~
:s
~
Q.,
Parasite Species
Figure 10. Percent of infections for the six most comon trematode
species infecting Cerithidea and Batillaria for all size classes in the
south marsh of Bolinas Lagoon. Data collected September 1995.
Snails were collected from the seven designated sampling stations.
Number of infected snails sampled are given. Error bars represent
the upper 95% C. I.
37
Table 5. Two - way ANOV A, incidence of infection. Susceptibility of
Cerithidea and Batillaria to ambient levels of free swimming miracidia in
Bolinas Lagoon.
Source
Size Class
Species
Size Class
x Species
Residual
ss
29.152
MS
117.383
29.152
F- Value
1.662
0.413
P- Value
0.2096
0.5267
1
22.197
22.197
0.314
0.5803
24
1695.203
70.633
df
1
1
117.383
DISCUSSION
The ability of Batillaria attramentaria to colonize various substrates and
to disperse rapidly exemplifies the weedy and invasive nature of many
introduced flora and fauna (Petraitis 1989; Carlton 1982, 1992; Carlton et al.
1990; Nichols et al. 1990; Buell et al. 1995). Variable substratum along the
lagoon's upper bank inhibits the movement of individuals limited to a
particular substrate type. Patches of mud and silt substrates were generally
bordered by sand or cobble sediments. If neither species could survive on
these margin substrata, B. attramentaria would still have an advantage to
disperse. Batillaria attramentaria travel greater distances per given time than
C. californica (Whitlatch and Obrebski 1980) and could potentially bypass
unsuitable substrate. However, B. attramentaria were able to exploit all
microhabitats. Large areas devoid of C. californica, yet accessible, were
inhabited by B. attramentaria. Morphological differences in feeding
structures between the two snails (Driscoll 1972) may dramatically influence
the range of substrate utilized, explaining a portion of the observed
distribution variability. Cerithidea californica has evolved a feeding structure
specialized for fine grain food particles (Driscoll 1972), evidently limiting its
capability to obtain sufficient food particles to specific substrates. The
intermittent nature of suitable substratum has isolated metapopulations of C.
californica throughout Bolinas Lagoon. Conversely, the ubiquity of B.
attramentaria is enhanced by its increased mobility and less specialized
feeding structures (Driscoll 1972) which allow the utilization of an array of
substrata. As seen in the overall distribution changes within Bolinas Lagoon
between September 1994 and April 1996, C. californica showed a stable, patchy
39
distribution while the distribution of B. attramentaria was more dynamic and
continuous. Batillaria attramentaria has the potential of colonizing all edges of
the lagoon and the Pine Gulch Creek delta.
Temporal density changes within the south marsh indicated a decrease
in C. californica between reproductive seasons with only marginal increases in
the density of B. attramentaria. Several factors may combine to explain this
trend. The density of C. californica decreased with the winter low activity
period, when the snails bury into the mud for the season. Cerithidea californica
densities did not return to pre-winter levels in the spring as did levels of B.
attramentaria, suggesting low survivability of C. californica to seasonal
extremes of environmental conditions. The mortality of C. californica is
facilitated by increased parasitic infection and ambient density. Parasitic
infection lowers survivorship in extreme environmental conditions such as
anoxia (Sousa and Gleason 1989). Therefore a greater number of C. californica
are expected to not survive the winter due to the probability of parasitic
infection alone. Since B. attramentaria have a lower parasitic prevalence
compared with C. californica, and are resistant to the influence of increased
interaction, it is expected that B. attramentaria populations can tolerate
extreme winter conditions.
Whitlatch and Obrebski (1980) suggest that juvenile B. attramentaria
compete for resources with mature C. californica. Seasonal removal of C.
californica (e.g., through mortality) possibly reduces resource competition,
abating constraints of sympatry for juvenile B. attramentaria. As individual B.
attramentaria colonize space voided by mortality, particularly maturing
juveniles, the density of B. attramentaria increases. The negative effects of
density on C. californica eventually magnify over the population. A negative
40
feedback cycle of increasing C. californica mortality with increasing B.
attramentaria density ensue.
Similarly, a cyclical interference ("bullying") displacement of C.
californica by Ilyanassa obsoleta (Race 1979, 1982) occurs in San Francisco Bay.
Ilyanassa obsoleta seasonally invade and retreat from the mudflats. As they
invade, C. californica are physically forced into microhabitat refuges I. obsoleta
do not occupy. Populations of C. californica survive in San Francisco Bay
because I. obsoleta cannot survive in the upper distribution limits of C.
californica. On the New England coast, Brenchley and Carlton (1983) describe
a density - related interference interaction between I. obsoleta and the
introduced European gastropod Littorina littorea. As the intensity of
interaction with L. littorea increases, I. obsoleta migrate to habitat free of
interspecific interaction. Again, the invading species is limited by substrate,
creating permanent refuge from complete displacement. The emigration
response is limited to adults; I. obsoleta and L. littorea juveniles have similar
feeding preferences and avoidance has not been noted in juvenile I. obsoleta.
In contrast, C. californica in Tomales Bay and Bolinas lagoon do not have
microhabitats to escape complete displacement. Batillaria attramentaria were
observed in all microhabitats C. californica occupied and those microhabitats
C. californica did not occupy.
Density decreases between seasons for both snail species may be a
result of the heavy rains in the 1994-1995 winter season. Both mud snails have
a tolerance for extreme salinity fluctuations over long periods of time (Race
1981, pers. obs.), however the extended flooding resultant from heavy winter
may have surpassed this limit. The temporal data from this study do not
incorporate the community dynamics of parasitic infection or size structure
41
for pre and post winter sampling. These data are relevant when placed into
the context of seasonal weather conditions (Race 1981, Sousa and Gleason
1989). Therefore, the trend noted in the temporal data may have been
bolstered by extreme environmental conditions.
McCloy (1979) indicated greater migration and mortality with
increased intraspecific interaction of C. californica in a southern California salt
marsh. An ability to thrive in extreme densities may be B. attramentaria's
principal means of dominating new habitats. The density data for C.
californica reported in Lafferty (1993a) in the Carpinteria Salt Marsh Reserve, in
southern California, were estimated to be 360/m2. Sympatric populations in
Tomales Bay were reported to be approximately 300jm2 during the early
1970's (Whitlatch and Obrebski 1980) and an estimated 700jm2 from Bolinas
Lagoon. Density estimates up to 1300jm2 B. attramentaria have been found in
Elkhorn Slough, California and over 5000 I m2 in Bolinas Lagoon (McDermott,
unpublished data 1994). Lower B. attramentaria density estimates were
observed in Millerton Marsh (76.5jm2) and Walker Creek (104.9jm2) in
Tomales Bay (Whitlatch 1974). The population structure in these extreme
density zones is dominated by size classes< 20 mm. Although small B.
attramentaria may be more efficient at collecting limited food material at high
densities, the reduced size frequency distribution may be a response to the
limited food supply.
Parasitic castration, by nature, significantly reduces the reproductive
output of afflicted populations (Kuris 1974, May 1983, Kabat 1986, Blower and
Roughgarden 1987). If the fecundity of C. californica and B. attramentaria is
relatively equal, the density dependent mortality mechanism of displacement
should continue as described above. However, differential infection was
42
determined among age groups and the influence of parasitic castrators may
regulate the displacement. The prevalence of younger C. californica was
greater than similar size B. attramentaria, decreasing the potential
reproductive output of newly matured C. californica. In addition, prevalence
decreases between the smallest and the mid size classes. Individuals do not
lose infections once infected (Sousa 1983), suggesting mortality of infected C.
californica for individuals 15.00 to 16.99 mm is elevated compared to larger C.
californica. The increased mortality may be directly related to parasitic
castration. Altered size frequency distributions attributed to the observed
differential prevalence or altered feeding habits caused by parasite infection
(Curtis and Hurd 1983) have not been tested. The effects of early infection
may enhance the displacement cycle.
Seasonality of parasite prevalence (Martin 1955, Sousa 1983) and of the
most common trematode species (Yoshino 1975) may influence the observed
parasite prevalence within the south marsh. Sousa (1983) detected an
increased parasite prevalence for smaller sized individuals (15-18 mm C.
californica) during the 1991 sampling period versus the 1990 sampling period.
This difference was attributed to a greater abundance of the trematode
Echinoparyphium in 1991. The difference in parasite prevalence between C.
californica and B. attramentaria in the south marsh may be related to a seasonal
abundance of Parorchis acanthus, the most common trematode species
infecting C. californica, or Euhaplorchis californiensis, the most common
trematode species infecting B. attramentaria. An anomalous increase or
decrease of P. acanthus or E. californiensis during the summer of 1995 could
have significantly altered the data interpretation.
43
In addition, effects on the physiology of C. californica varies with
parasite species and with the maturity of the snail (Sousa 1983). Euhaplorchis
californiensis and Parorchis acanthus have similar effects on the growth of adult
C. californica (Sousa 1983). Within allopatric subpopulations of C. californica,
parasite- induced behavioral modifications of the snail have not been
documented, except the absence of copulatory behavior (Sousa 1983).
Behavior modifications of these snails may be subtle and vary with parasite
species (Holmes and Bethel1972, Curtis and Hurd 1983, Curtis 1987, 1990,
Brown et al. 1988).
Conflicting results were obtained from the parasite prevalence survey
in the south marsh and the susceptibility study. Cerithidea californica and B.
attramentaria from allopatric areas had similar prevalence levels, however, C.
californica from sympatric subpopulations had greater parasite prevalence
than coexisting B. attramentaria, suggesting a greater susceptibility of C.
californica. Uninfected snails subjected to free swimming miracidia and
trematode eggs in ambient conditions did not produce a differential
incidence of infection. The larger size class used, similar in size to snails in
the second year of maturity, were no more susceptible than smaller
individuals. Therefore, infection would be more related to exposure time
than factors related to the snail species or degree of maturity.
Environmental factors significantly influence maturation size (McCloy
1979, Race 1981, Sousa 1983, Lafferty 1993b). If immature individuals were
impervious to mortality, delayed maturation of juveniles would be a
reasonable mechanism to ensure survival (Barclay and Gregory 1982).
Similarly, if large individuals were immune to outside factors such as
predation, selection would favor individuals that can postpone maturity at
44
the expense of increased growth in the presence of predators (Crowl and
Covich 1990). Lafferty (1993b) suggested that juvenile Cerithidea californica
mature earlier in areas of high parasitic prevalence compared to juveniles
from areas of lesser prevalence. Cerithidea californica and B. attramentaria both
develop reproductive capabilities at approximately 2 years; however,
maturation sizes are not compatible. After 2 years, C. californica from southern
and central California attain 18-22 mm (McCloy 1979, Race 1981, Sousa 1983),
whereas B. attramentaria from British Columbia range from 9 to 15 mm
(Whitlatch 1974, Yamada 1982). These differences may be related to
temperature variation at different latitudes.
The observed difference in percent infection within the south marsh of
Bolinas Lagoon may be related to size of maturity. Spatial and temporal
variability of parasite prevalence was eliminated by evaluating prevalence for
both snails at the same time and within the same space. The percent of
infected C. californica in smaller size classes was greater. Apparently, B.
attramentaria in Bolinas Lagoon mature at larger sizes than coexisting C.
californica in Bolinas Lagoon. Immature B. attramentaria 16.00 - 17.99 mm were
2.9 times more common then immature C. californica of the same size class.
Whether the larger B. attramentaria maturation size is a response to parasitism
or the result of latitudinal differences or a combination of factors is not
certain.
Disturbance of the substrate offers new resource availability to
organisms with proficient response mechanisms (Oliver and Slattery 1985,
Oliver et al. 1985). Small scale disturbances, such as animal activity or wrack
washed into the marsh with flood tide, where small areas of substrata are
impacted, creates optimal habitat for new diatom growth by removing
45
grazers and releasing nutrients otherwise contained within the substrata. The
mobility of B. attramentaria allows individuals to effectively colonize this
plethora of diatoms; B. attramentaria colonized disturbance patches in
abundance's exceeding ambient dispersal patterns. Cerithidea califomica
eventually migrate into impacted areas, more likely the result of dispersal
patterns unrelated to the disturbance.
Anthropogenic activity is the primary disturbance mechanism in the
south marsh. Footprints and dredging create short - and long - term
disturbances. Small depressions persist as long as 2 months. Dredging of fill
material adjacent to the south marsh, November 1993, initiated a long - term
erosional disturbance. Exposing the marsh to increased tidal flux reversed
the observed depositional pattern (Rowntree 1973, Berquist 1978, 1979). The
new erosional trend will ultimately alter the sediment composition (Liu and
Zarillo 1993) which may lead to reducing the competitive ability of C.
californica. As observed in other locations in the marsh, C. californica does not
thrive in microhabitats other than silt and mud. If the new tidal regime were
to eliminate fine silts, leaving course substrate, C. californica may be left to
isolated refuges. Batillaria attramentaria is abundant in the dredged areas.
Recruits most certainly originated from the edge of the lagoon where
densities were in excess of 5000 per m2 (pers. obs.). The silty-mud substratum
is similar to that of mudflats surrounding the dredge site. Cerithidea californica
are absent from the dredge areas although the substratum is suitable. It may
be possible that B. attramentaria from the area surrounding the dredge site
migrated into the newly established mudflat in numbers too vast for C.
californica to compete. Alternatively, C. californica is less mobile and will
eventually occupy the dredge site.
46
Environmental implications of B. attramentaria invasion may extend
well beyond the probable elimination of a native gastropod from its northern
range, although this may be the most visible outcome. The resistance of B.
attramentaria to an array of environmental stresses and an ability to colonize
new habitat quickly give B. attramentaria the ability to influence the entire
community setting it has invaded. The most profound feature of B.
attramentaria's presence is its capability to maintain extremely high densities,
which undoubtedly modifies the epifaunal, infaunal, and algae community
dynamics. Similar to B. attramentaria is the recent invasion and explosive
population expansion of the bivalve Potamocorbula amurensis into San
Francisco Bay (Carlton et al. 1990, Nichols et al. 1990). Within 10 years of
introduction, P. amurensis has affected all levels of the estuarine community
(Carlton et al. 1990). As a bioturbator, P. amurensis limits both infaunal
recruitment by altering substrate dynamics and turbulence over the substrate
(Carlton et al. 1990); as a filter feeder, P. amurensis removes copepod nauplii,
bacteria, phytoplankton, and planktonic larvae (Nichols et al. 1990). Other
introduced bivalves, including Gemma gemma observed in Bolinas Lagoon,
have similar potential to alter community dynamics but remain
uninvestigated (Carlton 1992). Reductions of infaunal recruitment have been
associated with deposit feeding gastropods, such as Ilyanassa obsoleta (Hunt et
al. 1987). Ilyanassa obsoleta are able to influence an array of infaunal species by
the diverse mechanisms of interaction the snail demonstrates. Seasonal
densities range between 100 to approximately 1000 per m2 and the greatest
effect on the infaunal community is expected during the snail's high density
summer months (Hunt et al. 1987). Polychaete infaunallarvae and juveniles
(including Cirratulidae, Capitellidae and Spionidae, taxa common in Bolinas
47
Lagoon) on the substrate surface are most affected by I. obsoleta; predation and
sediment disturbance potentially alter larval settlement patterns (Curtis and
Hurd 1979, Brenchley 1981, Woodin 1985).
Exclusion of juvenile B. attramentaria by adult sympatric C. californica
has been suggested as a mechanism to reduce competition for food resources
(Whitlatch and Obrebski 1980). This indicated competition between adults
and juveniles suggests coexistence of juvenile and adult C. californica with
adult B. attramentaria. Differential mortality and sensitivity to intra- and
interspecific interaction, however, were not taken into account as long- term
mechanisms of displacing C. californica. In addition, parasites have not been
evaluated as mediators of interaction and competition. This is of particular
importance when evaluating interaction. Parasite prevalence for C. californica
and B. attramentaria was greater in sympatric subpopulations compared with
allopatric subpopulations. The parasites may enhance the density dependent mortality cycle, facilitating the long - term displacement of C.
californica. However, a refuge for C. californica to survive the invasion of B.
attramentaria could be found in sympatry. High parasite prevalence has been
correlated with lower density (Lafferty 1993a). A lower density of both
species would decrease interactions to a level that does not negatively affect
C. californica. The observation that trematode prevalence is higher in areas of
sympatry supports this hypothesis.
It appears interaction has negatively influenced C. californica
populations in Tomales Bay. Populations of C. californica in Tomales Bay are
rare and those existing are sympatric with B. attramentaria. A survey of
Tomales Bay in July 1996 revealed two small subpopulations of C. californica:
one on the southwestern bank at Indian Lagoon and one on Millerton Marsh
48
(Byers and McDermott, in prep.). The subpopulation C. californica on
Millerton Marsh was documented to coexist with B. attramentaria in the early
1970's (Whitlatch and Obrebski 1980). The 1996 survey showed low densities
Cerithidea californica in this area and individuals were generally large, > 18 mm
(Byers and McDermott, in prep.). Previous species density data were not
obtained, therefore changes in species ratio over time could not be evaluated.
The population structure of coexisting C. californica and B. attramentaria in
Tomales Bay may indicate the future of C. californica in Bolinas Lagoon.
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APPENDICES
APPENDIX A
TEMPORAL DENSITY DATA
APRIL 1994 - AUGUST 1995
Temporal ~itsity Data
Snail counts from 6 subsample 23x23 em quadrats to estimate density at each sampling station within the south marsh of Bolinas Lagoon.
Stations were sampled quarterly from April1994 to August 1995. Density values are given with a station mean and standard error calculated
for each sampling period.
Date
Station
1
Cerithidea
26-Apr-94
26-Apr-94
26-Apr-94
26-Apr-94
26-Apr-94
26-Apr-94
Station Mean
Standard Error
12-Sep-94
12-Sep-94
12-Sep-94
12-Sep-94
12-Sep-94
12-Sep-94
Station Mean
Standard Error
Cerithidea
4
3
2
Batillaria
Batillaria
Cerithidea
Batillaria
Cerithidea
Batillaria
25
17
45
28
33
38
3
16
30
32
15
40
10
5
12
17
23
30
11
16
14
22
36
6
35
33
26
22
20
27
14
1
7
5
3
10
17
9
13
22
19
16
12
9
8
9
6
20
31.00
4.04
22.67
5.57
16.17
3.74
17.50
4.29
27.17
2.41
6.67
1.94
16.00
1.86
10.67
2.03
21
19
31
40
45
41
23
12
11
8
17
2
20
19
21
18
14
10
14
32
10
26
16
12
7
9
5
6
15
30
19
21
15
20
36
31
20
16
14
24
35
12
17
9
11
11
9
32.83
4.48
12.17
2.96
17.00
1.71
18.00
3.69
9.00
1.57
23.50
3.21
23.33
3.40
11.50
1.20
10
VI
00
Temporal~sity Data
Date
Station
1
2
4
3
21-0ct-94
21-0ct-94
15
37
3
1
13
22
16
33
17
25
13
9
17
12
10
7
21-0ct-94
21-0ct-94
21-0ct-94
20
22
13
15
38
8
16
18
13
43
30
36
2
8
52
12
32
4
36
24
19
1
2
9
21-0ct-94
15
19
12
25
22
32
41
6
Station Mean
20.33
14.00
15.67
30.50
21.00
17.00
24.83
5.83
Standard Error
3.61
5.56
1.56
3.80
7.13
4.91
4.64
1.49
24-Feb-95
44
1
25
26
4
0
2
3
24-Feb-95
24-Feb-95
24-Feb-95
24-Feb-95
24-Feb-95
40
46
14
46
40
16
3
10
1
7
10
13
4
18
15
1
12
1
129
0
4
7
3
14
0
3
3
12
5
14
9
7
4
24
0
0
19
5
11
Station Mean
38.33
6.33
14.17
28.17
5.33
6.17
9.33
6.33
Standard Error
4.99
2.42
2.91
20.58
1.96
2.27
3.18
3.03
12-May-95
52
9
3
2
5
4
11
48
12-May-95
12-May-95
12-May-95
12-May-95
12-May-95
42
44
22
36
13
7
4
21
11
3
4
0
0
0
1
7
8
3
2
0
4
13
10
18
3
6
13
12
19
6
14
21
22
9
39
35
33
26
18
25
10
Vl
\0
Temporalinsity Data
Date
Station
1
2
4
3
Station Mean
34.83
9.17
1.33
3.67
8.83
10.00
19.33
30.83
Standard Error
5.98
2.66
0.71
1.28
2.41
2.32
4.48
4.24
18
21
13
20
14
17
19
35
22
43
20
18
5
10
3
9
8
10
23
23
32
33
24
22
16
11
13
18
23
14
32
14
17
24
5
5
7
9
6
9
13
2
5
8
12
13
5
19
17.17
1.30
26.17
4.22
7.50
1.18
26.17
2.02
15.83
1.74
16.17
4.35
7.67
1.50
10.33
2.22
15-Aug-95
15-Aug-95
15-Aug-95
15-Aug-95
15-Aug-95
15-Aug-95
Station Mean
Standard Error
0\
0
APPENDIXB
COLONIZATION DATA
Colonization of Available Substrate
Data for the colonization study in the south marsh of Bolinas Lagoon. Values represent weekly subsample data from each of six 20x20cm
quadrats used to evaluate the colonization manipulation plots. Data were collected as number of snails per ~drat.
Sampling Period
Date
Station
2
1
3
Cerithidea
Batillaria
Cerithidea
Batillaria
Cerithidea
Batillaria
4
4
2
8
3
4
4
4
4
4
8
5
7
19
6
8
5
4
6
4
3
3
6
3
8
6
5
5
2
6
8
16
7
22
Control Plot
Week#1
30-Sep-95
30-Sep-95
30-Sep-95
30-Sep-95
30-Sep-95
30-Sep-95
10
10
Week#2
8-0ct-95
8-0ct-95
8-0ct-95
8-0ct-95
8-0ct-95
8-0ct-95
1
2
1
0
4
1
2
0
1
0
1
0
1
0
0
1
0
0
0
0
9
1
2
4
3
3
3
1
1
0
12
2
7
3
5
3
Week#3
14-0ct-95
14-0ct-95
14-0ct-95
1
1
3
0
1
0
4
2
0
4
3
1
8
3
6
20
21
8
0\
N
Colonization of A vLable Substrate
Sampling Period
Date
Station
2
1
Week#4
3
14-0ct-95
14-0ct-95
0
1
5
0
1
0
4
5
5
5
12
14-0ct-95
1
0
2
4
4
10
21-0ct-95
21-0ct-95
21-0ct-95
21-0ct-95
21-0ct-95
21-0ct-95
3
0
2
3
3
6
1
3
1
6
2
1
2
1
3
1
1
1
1
2
4
2
7
4
3
1
2
1
0
5
13
6
3
9
30-Sep-95
30-Sep-95
30-Sep-95
30-Sep-95
30-Sep-95
30-Sep-95
1
3
3
3
13
31
3
8
6
5
3
6
2
2
2
1
4
1
4
2
2
2
12
26
6
6
11
3
14
4
10
6
0
9
23
9
8-0ct-95
8-0ct-95
2
0
0
1
0
2
24
25
0
0
3
3
10
4
9
Low Impact (Picked) Plot
Week#1
Week#2
0\
w
Sampling Period
Colonization of A vLable Substrate
Station
2
Date
1
Week#3
Week#4
3
Cerithidea
Batillaria
Cerithidea
Batillaria
Cerithidea
Batillaria
8-0ct-95
8-0ct-95
8-0ct-95
8-0ct-95
1
0
0
2
1
i
0
0
1
0
2
0
9
6
0
1
0
i
0
1
7
4
4
8
14-0ct-95
14-0ct-95
14-0ct-95
14-0ct-95
14-0ct-95
14-0ct-95
1
0
2
0
3
4
0
1
0
11
0
3
3
4
4
2
6
1
11
11
11
16
12
9
0
3
3
2
2
1
12
9
7
15
2
10
21-0ct-95
21-0ct-95
21-0ct-95
21-0ct-95
21-0ct-95
21-0ct-95
5
4
2
2
5
4
0
5
12
9
6
13
1
8
1
3
1
3
5
0
3
0
3
3
0
12
12
12
12
14
8
0
3
0
0
0
0
0
2
0
7
5
1
High Impact (Cleared) Plot
Week#1
30-Sep-95
30-Sep-95
30-Sep-95
3
1
3
5
5
4
4
3
7
26
13
Cl\
..j::.
Sampling Period
{tation
Date
2
1
3
Cerithidea
Batillaria
Cerithidea
Batillaria
Cerithidea
Batillaria
30-Sep-95
30-Sep-95
30-Sep-95
0
1
1
0
0
0
0
1
1
2
1
0
3
4
2
8
16
8
Week#2
8-0ct-95
8-0ct-95
8-0ct-95
8-0ct-95
8-0ct-95
8-0ct-95
1
1
0
0
0
0
3
0
0
0
0
5
0
0
1
0
2
1
3
6
6
0
3
5
0
0
0
0
1
0
1
3
1
1
3
15
Week#3
14-0ct-95
14-0ct-95
14-0ct-95
14-0ct-95
14-0ct-95
14-0ct-95
0
1
0
0
1
1
3
3
1
0
2
6
0
1
1
1
2
1
2
3
6
1
3
8
4
3
5
11
5
3
6
18
15
11
8
21-0ct-95
21-0ct-95
21-0ct-95
21-0ct-95
21-0ct-95
21-0ct-95
0
1
1
0
2
2
1
1
1
1
3
1
1
0
0
1
0
0
1
1
0
0
2
3
1
0
2
0
1
0
8
10
10
12
11
11
Week#4
0\
Vl
APPENDIXC
SIZE FREQUENCY DISTRIBUTION AND DENSITY DATA
Percent Size Frequency Distribution
an~ensity
Data
Size frequency distribution and density data for each of seven stations in the south marsh of Bolinas Lagoon used in the intraspecific
interaction study. Population dynamics were estimated in July 1995.
Station#
Size Class
(mm)
1
Cerithidea
% Size Frequency
Batillaria
% Size Frequency
Mean#/23x23 em
Cerithidea
Mean# /23x23 em
Batillaria
Mean#/23x23 em
Total
12
10
22
30
6
3
17
12
7
1
24
17
17
33
13
22
29
26
8
14
31
45
15-16
17-18
19-20
21-22
23-24
25-26
27-28
29-30
1
2
1
6
18
17
14
2
10
7
14
13
2
15-16
17-18
19-20
21-22
23-24
25-26
27-28
29-30
9
3
2
14
23
32
10
7
3
15-16
17-18
19-20
21-22
23-24
2
8
22
40
19
10
2
2
5
0\
-..]
Percent Size Frequency Distribution anloensity Data
Station#
4
5
6
Size Class
(mm)
Cerithidea
% Size Frequency
Batillaria
% Size Frequency
25-26
27-28
5
2
2
0
29-30
1
0
15-16
17-18
19-20
21-22
23-24
4
16
23
35
16
36
27
20
8
4
25-26
27-28
29-30
5
1
0
2
1
2
15-16
17-18
19-20
21-22
23-24
1
4
7
16
26
30
31
19
11
7
25-26
27-28
29-30
29
12
5
1
1
0
15-16
17-18
19-20
0
0
0
12
17
25
Mean# /23x23 em
Cerithidea
Mean# /23x23 em
Batillaria
Mean# /23x23 em
Total
18
15
33
12
15
27
2
28
30
0\
00
Percent Size Frequency Distribution and lensity Data
Station#
7
Size Class
(mm)
Cerithidea
% Size Frequency
21-22
23-24
25-26
27-28
29-30
30
10
20
30
15-16
17-18
19-20
21-22
23-24
25-26
27-28
29-30
1
0
3
17
27
27
15
10
10
Batillaria
% Size Frequency
Mean# /23x23 ern
Cerithidea
Mean#/23x23 em
Batillaria
Mean #/23x23 em
Total
20
9
4
4
9
51
25
9
8
5
2
0
0
11
13
24
APPENDIXD
SHELL GROWTH DATA
Growth Rate Data and Infection Status
s~marsh
Growth data for the density manipulations conducted in the
of Bolinas Lagoon. Data are given as: the initial growth measured
as shell length at the begining of the study; final growth measured as shell length at the end of the study; and shell production measured as
the amount of shell produced at the mantle edge. Infection status is noted.
Station
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
Density
Treatment
Snail
Species
Initial Size (rnrn)
21-Jul-95
Final Size (rnrn)
30-Sep-95
Shell Growth
(rnrn)
Shell Production
(mm)
Infected (P)
Uninfected (N)
Low
Low
Low
Low
Low
Low
Low
High
High
High
High
High
High
High
High
High
High
High
High
High
High
Control
Batillaria
Batillaria
Batillaria
Cerithidea
Ceritlzidea
Cerithidea
Cerithidea
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Batillaria
20.14
22.66
21.58
24.2
22.5
22.48
23.2
20.68
20.98
20.1
21.28
22
21.9
22.84
22.7
24.74
23.9
21.4
24.8
22.22
23.5
24.06
22.6
25.5
21.95
26.7
25.35
26.45
25.45
21.85
21.45
23.6
24.25
22.55
22.55
23.8
25.9
24.74
24.5
25.55
26
24.6
25.35
24.25
2.46
2.84
0.37
2.5
2.85
3.97
2.25
1.17
0.47
3.5
2.97
0.55
0.65
0.96
3.2
0
0.6
4.15
1.2
2.38
1.85
0.19
12.01
12.35
3.8
13.35
11
5.45
13.8
5
3.15
7
3.75
5
4.2
N
N
N
N
N
N
N
N
N
**
N
10
p
9.4
N
N
N
N
N
N
N
**
17.9
9.75
13.5
11.95
**
p
N
p
p
..._j
.......
Growth Rate Data and Infection Status
/
Station
Density
Treatment
Snail
Species
Initial Size
21-Jul-95
1
1
1
1
1
Control
Control
Control
Control
Control
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
Low
Low
Low
Low
Low
Low
Low
High
High
High
High
High
High
High
Low
Low
Low
Low
High
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Ceritlzidea
/
FinalSize
Shell Growth
(mrn)
Shell Production
30-Sep-95
23.2
22.16
21.2
23
22.5
26.2
22.3
22.25
23.8
23.7
3
0.14
1.05
0.8
1.2
10.55
0
9
6.7
10.2
20.5
21.58
21.3
24.9
22.66
20.1
21.98
22.22
21.18
21.24
24.62
20
20.4
20.66
20.9
23.7
23.7
23.6
21.58
23.3
23.6
22.55
25.4
24.25
25.4
25.8
24.9
23.7
21.35
25.15
24.25
22.1
24.35
21.8
24.95
24.5
24.25
22.9
2.8
2.02
1.25
0.5
1.59
5.3
3.82
2.68
2.52
0.11
0.53
4.25
1.7
3.69
0.9
1.25
0.8
0.65
1.32
**
(rnrn)
11.15
9.25
**
**
**
**
**
9.65
2.3
8.25
20.65
**
**
7
10
**
5
**
Infected (P)
Uninfected (N)
p
N
N
N
N
N
N
N
N
N
N
p
N
N
p
N
N
N
N
N
N
N
N
N
-.l
N
Growth Rate Data and Infecti~Status
Station
Density
Treatment
Snail
Species
Initial Size
21-Jul-95
Final Size
30-Sep-95
Shell Growth
(nun)
Shell Production
(mm)
Infected (P)
Uninfected (N)
2
2
2
2
2
2
2
2
2
2
2
2
High
High
High
High
High
High
High
High
Control
Control
Control
Control
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Batillaria
Batillaria
Batillaria
Cerithidea
24.54
23.5
23
23.34
23.56
23.9
22.46
23.82
21.38
21.12
20
23.8
26
24.55
24.75
24.4
23.8
23.8
22.45
23.7
24.9
25.6
24.55
23.9
1.46
1.05
1.75
1.06
0.24
0
0
0
3.52
4.48
4.55
0.1
7
N
N
N
N
N
N
3
3
3
3
3
3
3
3
3
3
Low
Low
Low
Low
Low
Low
High
High
Low
Low
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Cerithidea
Cerithidea
22.16
21.32
22.64
21.2
21.66
22.68
20.7
21.4
22.76
22.78
23
22
23.15
23.95
23.05
23.55
21.15
22
23.8
25.1
0.84
0.68
0.51
2.75
1.39
0.87
0.45
0.6
1.04
2.32
**
**
6.2
1.7
0
0
0
**
**
**
**
**
3.05
3.3
**
**
7
5
3.5
**
**
p
N
N
N
N
N
N
N
N
N
p
N
N
N
N
N
--J
U-l
Growth Rate Data a~fection Status
Station
3
3
3
3
3
3
3
3
3
3
3
3
3
3
3
3
3
3
3
3
3
3
3
3
3
3
Density
Treatment
Snail
Species
Initial Size
21-Jul-95
Final Size
30-Sep-95
Shell Growth
(mrn)
Shell Production
(mrn)
Infected (P)
Uninfected (N)
Low
Low
Low
Low
Low
High
High
High
High
High
High
High
High
High
Control
Control
Control
Control
Control
Control
Control
Control
Control
Control
Control
Control
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Batillaria
Batillaria
Bat ill aria
Batillaria
Batillaria
Batillaria
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
21.08
21.2
21.44
24.5
22.36
20
20.22
22.8
22.46
21.58
21.42
21.84
20.1
22.5
22.3
22.66
21
22.12
22.6
20.94
21.18
21.46
22.38
21.34
20.18
20.2
23.7
23.4
23.6
27
23.8
23.3
20.45
23.1
22.95
23.3
23.15
22.65
22.35
23.6
23.3
23.4
21.85
23.5
23.75
22.15
22.2
21.65
23.45
22.6
22
20
2.62
2.2
2.16
2.5
1.44
3.3
0.23
0.3
0.49
1.72
1.73
0.81
2.25
1.1
1
0.74
0.85
1.38
1.15
1.21
1.02
0.19
1.07
1.26
1.82
0
**
**
**
**
**
**
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
p
4.4
**
**
**
**
3.8
**
**
**
**
**
**
**
**
**
**
**
**
**
0
-....]
..j:::.
Growth Rate Data apdfufection Status
Station
Density
Treatment
Snail
Species
Initial Size
21-Jul-95
Final Size
30-Sep-95
Shell Growth
3
3
Control
Control
Cerithidea
Cerithidea
22.1
23
21.75
22.65
0
0
4
4
4
4
4
4
4
4
4
4
4
4
4
4
4
4
4
4
4
4
4
Low
Low
Low
Low
Low
Low
Low
Low
High
High
High
High
High
High
High
High
High
High
High
Control
Control
Batillaria
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Ceritltidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Batillaria
Cerithidea
20.18
22.56
21.32
21
23.42
21
22.16
21.04
21.96
20.5
21.7
21.98
22
20.1
20.84
23.2
22.82
21.18
21.36
21.78
20.38
21.35
23.65
22.2
23
25.15
22.25
23.55
20.85
22.05
20.5
21.85
21.7
21.7
21.5
21.6
22.9
22.55
21
22.1
21.05
22.1
1.17
1.09
0.88
2
1.73
1.25
1.39
0
0.09
0
0.15
0
0
1.4
0.76
0
0
0
0.74
0
1.72
(nun)
Shell Production
(rnm)
Infected (P)
Uninfected (N)
0
N
N
**
**
**
7.3
9.2
10.55
**
**
0
**
**
**
N
N
N
N
N
N
N
N
p
0
0
0
0
0
N
N
N
N
N
N
N
N
N
N
N
**
N
0
0
4.45
**
-.]
Vt
Growth Rate Data ~fection Status
Station
Density
Treatment
Snail
Species
Initial Size
21-Jul-95
Final Size
30-Sep-95
Shell Growth
Shell Production
(mm)
(mm)
Infected (P)
Uninfected (N)
4
4
4
Control
Control
Control
Cerithidea
Cerithidea
Cerithidea
20.08
21.56
21.64
21.75
21.56
21.5
1.67
0
0
0
N
**
p
0
N
5
5
5
5
5
5
5
5
5
Low
Low
Low
High
High
High
Control
Control
Control
Batillaria
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Batillaria
Cerithidea
Cerithidea
24.82
23.66
20.18
24.58
24.32
22.38
20.8
23.28
23.28
24.6
24.35
21.4
24.25
24.5
23.6
24.3
23
26.4
0
0.69
1.22
0
0.18
1.22
3.5
0
3.12
**
**
**
**
**
**
**
**
**
N
N
N
N
N
N
p
6
6
6
6
6
6
6
6
6
6
6
Low
Low
High
High
High
High
High
High
High
Low
High
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Batillaria
Cerithidea
Cerithidea
23.4
24.42
22.4
22.1
22.4
20.1
20.6
21.52
24
24.32
22.28
25.1
25.22
25
23.3
25.25
23.35
24.35
25.35
26.2
24.15
22
1.7
0.8
2.6
1.2
2.85
3.25
3.75
3.83
2.2
0
0
12.35
3.75
p
**
**
**
**
**
**
**
**
0
N
N
N
N
N
N
N
N
p
p
N
N
-.J
0\
Growth Rate Data cm:e(Infection Status
Station
Density
Treatment
Snail
Species
Initial Size
21-Jul-95
Final Size
30-Sep-95
Shell Growth
(mm)
Shell Production
(mm)
Infected (P)
Uninfected (N)
6
6
6
High
Control
Control
Cerithidea
Batillaria
Batillaria
22.36
21.28
22.18
22.1
23
24.05
0
1.72
1.87
**
8
**
N
N
N
7
7
7
7
7
7
7
7
7
7
Low
Low
High
High
Low
Low
High
High
Control
Control
Batillaria
Batillaria
Batillaria
Batillaria
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
Cerithidea
21.8
22.9
22.7
23.22
22.36
20.88
22.6
24.06
22.76
24.64
22.5
23.2
25
23.3
23.7
21.2
22.2
23.75
23.4
25.25
0.7
0.3
2.3
0.08
1.34
0.32
0
0
0.64
0.61
9
**
**
6.1
10
**
**
**
**
**
N
**no shell production measurement
p
N
N
N
N
N
N
p
N
\
APPENDIXE
LAGOON PARASITE PREYALENCE DATA
Lagoon Parasite Preval~
Parasite prevalence data for various locations throughout Bolinas Lagoon. Snails were collected from
areas designated allopatric Cerithidea, allopatric Batillaria, or sympatric. Prevalence was calculated
for snails 20 - 25 mm and collected on12 September 1994.
Sympatric Subpopulations
Site
*4.3 km north
*1.0 km north
*0.6 km north
*0.6 km north
*0.4 km north
*0.4 km north
*0.1 km north
*0.1 km north
Channel Mouth
Channel Mouth
Marsh Front
Marsh Front
South Marsh, Station #2
South Marsh, Station #3
Snail Species
B
c
B
c
B
c
B
c
B
c
B
c
B
c
%infected
76
33.33
45
30
88.9
55.6
44.4
25
66.7
30
5
0
15
17
#infected
13
1
9
3
8
15
11
4
4
3
1
0
6
6
Sample Size
17
3
20
10
9
27
25
16
6
10
20
20
40
36
Allopatric Subpopulations
Pine Gulch Creek Delta
Pine Gulch Creek Delta
Audubon Canyon Ranch
*Panne, 4.2 km
*Turnout, 1.6 km
*0.2km
c
c
c
c
B
B
27.78
12.00
4.00
8.00
40.00
8.00
5.00
3.00
1.00
2.00
10.00
2.00
18.00
25.00
25.00
25.00
25.00
25.00
* distances are measured north from South Marsh
C = Cerithidea
B = Batillaria
00
0
\
APPENDIXF
SOUTH MARSH STUDY SITE PARASITE
PREVALENCE DATA
South Ma~Study Site Prevalence
Parasite prevalence data for the south marsh of Bolinas Lagoon. Data were collected in July and September of 1995.
Sampling
Date
Station#
Size
Class
Uninfected
15 Juy95
15 Juy95
1
2
Batillaria
Cerithidea
15-16.99
17-18.99
19-20.99
21-22.99
23-24.99
25-26.99
27-28.99
29-30.99
Overall
2
4
7
12
8
9
5
1
48
15-16.99
17-18.99
19-20.99
21-22.99
23-24.99
25-26.99
27-28.99
29-30.99
Overall
0
0
0
5
13
12
12
6
48
Parasitized
%Infected
Uninfected
Parasitized
%Infected
11
0.00
0.00
22.22
7.69
20.00
10.00
44.44
50.00
18.64
11
7
11
8
3
1
0
0
41
1
0
1
1
4
2
1
3
13
8.33
0.00
8.33
11.11
57.14
66.67
100.00
100.00
24.07
0
0
0
1
5
1
2
3
12
0
0
0
16.67
27.78
7.69
14.29
33.33
20.00
6
10
13
10
2
0
0
0
41
0
1
0
3
4
2
5
6
21
0.00
9.09
0.00
23.08
66.67
100.00
100.00
100.00
33.87
0
0
2
1
2
1
4
1
00
N
South M~Study Site Prevalence
Sampling
Date
Station#
Size
Class
Batillaria
Cerithidea
Parasitized
0
3
5
2
0
0
0
1
11
%Infected
0.00
75.00
45.45
12.50
0.00
0.00
0.00
50.00
18.64
Uninfected
4
11
18
9
6
2
0
0
50
Parasitized
0
1
1
5
1
0
0
0
8
%Infected
0.00
8.33
5.26
35.71
14.29
0.00
0.00
0.00
13.79
15 Juy95
3
15-16.99
17-18.99
19-20.99
21-22.99
23-24.99
25-26.99
27-28.99
29-30.99
Overall
Uninfected
0
1
6
14
22
3
1
1
48
15 Juy95
4
15-16.99
17-18.99
19-20.99
21-22.99
23-24.99
25-26.99
27-28.99
29-30.99
Overall
2
7
8
12
7
7
3
1
47
0
1
1
0
0
0
1
0
3
0.00
12.50
11.11
0.00
0.00
0.00
0.00
0.00
6.00
11
8
6
9
4
0
0
0
38
0
0
0
5
2
2
1
2
12
0.00
0.00
0.00
35.71
33.33
100.00
0.00
0.00
24.00
15 Juy 95
5
15-16.99
17-18.99
19-20.99
21-22.99
23-24.99
8
3
7
13
15
2
2
1
2
3
20.00
40.00
12.50
13.33
16.67
6
26
22
8
1
0
0
1
2
0
0.00
0.00
4.35
20.00
0.00
00
w
South MarslYStudy Site Prevalence
Sampling
Date
Station#
/
Size
Class
Batillaria
Cerithidea
25-26.99
27-28.99
29-30.99
Overall
Uninfected
8
1
0
55
Parasitized
1
0
0
11
%Infected
11.11
0.00
0.00
16.67
Uninfected
0
0
0
63
Parasitized
0
0
0
3
%Infected
0.00
0.00
0.00
4.55
15 Juy95
6
15-16.99
17-18.99
19-20.99
21-22.99
23-24.99
25-26.99
27-28.99
29-30.99
Overall
5
4
17
7
0
0
0
0
33
0
0
0
1
5
1
8
10
25
0.00
0.00
0.00
12.50
100.00
100.00
100.00
100.00
43.10
0
1
2
11
8
7
6
3
38
0
0
1
1
4
5
2
4
17
0.00
0.00
33.33
8.33
33.33
41.67
25.00
57.14
30.91
15 Juy95
7
15-16.99
17-18.99
19-20.99
21-22.99
23-24.99
25-26.99
27-28.99
0
0
1
6
10
17
8
0
0
0
2
2
0
0
0.00
0.00
0.00
25.00
16.67
0.00
0.00
13
9
11
13
3
3
0
0
0
1
4
2
2
3
0.00
0.00
8.33
23.53
40.00
40.00
100.00
00
..j::.
South Ma~£Study Site Prevalence
Sampling
Date
Station#
Size
Class
Cerithidea
Uninfectec Parasitized
Batillaria
%Infected
Uninfected
Parasitized
%Infected
29-30.99
Overall
0
42
1
5
100.00
10.64
0
52
3
15
100.00
22.39
30-Sep-95
1
15-16.99
17-18.99
19-20.99
21-22.99
23-24.99
25-26.99
27-28.99
29-30.99
Overall
2
3
4
14
19
15
15
12
84
1
2
3
5
8
2
1
3
25
33.33
40.00
42.86
26.32
29.63
11.76
6.25
20.00
22.94
19
15
19
22
19
12
8
1
115
0
0
1
1
6
1
2
8
19
0.00
0.00
5.00
4.35
24.00
7.69
20.00
88.89
14.18
30-Sep-95
2
15-16.99
17-18.99
19-20.99
21-22.99
23-24.99
25-26.99
27-28.99
29-30.99
1
0
2
4
8
15
15
18
0
0
1
6
6
6
2
3
0.00
0.00
33.33
60.00
42.86
28.57
11.76
14.29
2
7
12
14
19
12
7
5
0
0
0
1
3
0
2
3
0.00
0.00
0.00
6.67
13.64
0.00
22.22
37.50
00
VI
South Marsh Study Site Prevalence
Sampling
Date
Station#
Size
Class
Batillaria
Cerithidea
Uninfected
Parasitized
%Infected
Uninfected
Parasitized
%Infected
30-Sep-95
3
15-16.99
17-18.99
19-20.99
21-22.99
23-24.99
25-26.99
27-28.99
29-30.99
Overall
0
1
4
15
29
21
8
4
82
3
2
9
11
6
1
6
2
40
100.00
66.67
69.23
42.31
17.14
4.55
42.86
33.33
32.79
13
16
26
33
53
8
0
0
149
0
0
3
3
0
5
0
2
13
0.00
0.00
10.34
8.33
0.00
38.46
0.00
100.00
8.02
30-Sep-95
4
15-16.99
17-18.99
19-20.99
21-22.99
23-24.99
25-26.99
27-28.99
29-30.99
Overall
1
4
11
18
21
27
8
3
93
0
1
3
0
0
0
3
1
8
0.00
20.00
21.43
0.00
0.00
0.00
27.27
25.00
7.92
3
25
31
44
7
0
0
10
120
0
1
1
2
1
0
1
2
8
0.00
3.85
3.13
4.35
12.50
0.00
100.00
16.67
6.25
30-Sep-95
5
15-16.99
17-18.99
19-20.99
21-22.99
2
3
19
6
0
1
2
3
0.00
25.00
9.52
33.33
8
17
9
34
0
0
0
5
0.00
0.00
0.00
12.82
00
0\
South Marsh Study Site Prevalence
Sampling
Date
Station#
I
Size
Class
Batillaria
Cerithidea
Uninfected
Parasitized
%Infected
Uninfected
Parasitized
%Infected
23-24.99
25-26.99
27-28.99
29-30.99
Overall
13
23
15
9
90
1
0
2
5
14
7.14
0.00
11.76
35.71
13.46
33
4
2
0
107
1
0
0
0
6
2.94
0.00
0.00
0.00
5.31
30-Sep-95
6
15-16.99
17-18.99
19-20.99
21-22.99
23-24.99
25-26.99
27-28.99
29-30.99
Overall
0
0
0
0
1
3
3
6
13
0
0
0
0
0
0
0
0
0
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
14
11
21
30
27
12
5
0
120
0
0
1
1
3
7
9
16
37
0.00
0.00
4.55
3.23
10.00
36.84
64.29
100.00
23.57
30-Sep-95
7
15-16.99
17-18.99
19-20.99
21-22.99
23-24.99
25-26.99
27-28.99
29-30.99
Overall
0
0
1
10
20
13
9
0
1
2
4
5
1
1
5
19
0.00
100.00
66.67
28.57
20.00
7.14
10.00
35.71
23.46
12
17
24
24
22
0
0
1
3
4
2
0
5
15
0.00
0.00
4.00
11.11
15.38
16.67
0.00
100.00
12.10
9
62
10
0
0
109
00
-....]
\
APPENDIXG
INFECTING TREMATODE SPECIES DATA
Infecting Parasite Species
The six most common trematode species infecting Cerithidea californica and Batillaria attramentariain the south marsh of Bolinas lagoon.
Data were collected in September 1995.
Single Infections
Renicola cerithidicola
Euhaplorchis californiensis
Cloacitrema michiganensis
Parorchis acanthus
Mesostephanous appendiculatus
Pygidiopsoides spindalis
unidentified
Total infected
Total Uninfected
Batillaria
Cerithidea
Parasite Species
15-20.99mm
21-26.99mm
27-30.99mm
15-20.99mm
21-26.99mm
27-30.99mm
5
1
0
20
0
0
5
31
58
12
2
2
43
1
0
6
66
295
6
2
0
15
0
1
11
35
134
2
3
0
0
0
0
3
8
322
2
25
0
3
0
0
19
49
339
4
20
1
11
0
0
13
49
38
00
\0