JOURNAL OF CRUSTACEAN BIOLOGY, 30(2): 159-166, 2010
KILOMETER-SCALE SPATIAL VARIATION IN PREVALENCE OF THE RHIZOCEPHALAN
LERNAEODISCUS PORCELLANAE ON THE PORCELAIN CRAB PETROLISTHES CABRILLOI
Leah M. Sloan, Sarah V. Anderson, and Bruno Pernet
(LS; SVA; BP, correspondence, [email protected]) Department of Biological Sciences, California State University, Long Beach,
1250 Bellflower Blvd, Long Beach, California 90840, U.S.A.
ABSTRACT
We studied spatial variation in the prevalence of the rhizocephalan barnacle Lernaeodiscus porcellanae on its porcelain crab host,
Petrolisthes cabrilloi, at four southern California intertidal sites separated by only a few km. The prevalence of rhizocephalan externae
varied significantly among sites in 2008-2009, with the southernmost site, White Point, consistently showing higher prevalence than the
others. Externa prevalence was a good proxy of estimated true prevalence, i.e., the prevalence of rhizocephalans as a whole, not just
those that had formed externae. We examined several hypotheses that might explain the observed spatial variation in prevalence. Host
susceptibility to infection (indicated by the proxy of damage to host limbs, some of which are used to remove parasite infective stages),
did not differ among sites. At all sites, prevalence was slightly higher in female crabs than in males, and the sex ratio at White Point was
slightly female-biased while that at the other sites was male-biased; thus, among-site differences in sex ratio did contribute to observed
variation in prevalence. However, most spatial variation in prevalence appeared to be due to the effect of host size. At all sites the
probability of infection increased with increasing host size, and White Point crabs were on average much larger than crabs at other sites.
Overall, the size-class distribution of host crabs explained 80.4% of the variation in prevalence of L. porcellanae. Larger P. cabrilloi
have likely had greater opportunity to be infected by rhizocephalans, either because they are older, or because they have undergone more
molts, during which they are especially vulnerable to infection. A deeper understanding of small-scale spatial variation in prevalence in
L. porcellanae will require information on the causes of among-site variation in host population size structure.
KEY WORDS: barnacle, Lernaeodiscus porcellanae, parasitic castrator, Petrolisthes cabrilloi, Rhizocephala
DOI: 10.1651/09-3190.1
1988; Jeffery and Underwood, 2000) or biological (Gaines
and Roughgarden, 1987) determinants of propagule supply
to the habitat, the distribution of available habitat (Pineda,
1994), and interactions with previously-established conspecific or heterospecific competitors (Connell, 1961;
Bertness, 1981). In the context of parasite recruitment,
‘‘available habitat’’ represents hosts that can be successfully
infected, a parameter that is sometimes affected by host
age, reproductive status, and defenses (Rohde, 1984). All of
these factors can play roles in determining the prevalence
of parasitic castrators (Jokela and Lively, 1995; Alvarez et
al., 2001; Smith, 2007). However, identifying which is
most important in a given case is often challenging. In
parasites with complex life histories, the local abundance of
definitive hosts sometimes explains much of the variation
in prevalence in intermediate hosts (Williams and Esch,
1991; Latham and Poulin, 2003; Smith, 2007). Because
definitive hosts are the source of parasite propagules that
might infect intermediate hosts, this suggests that propagule
supply is an important determinant of prevalence in
intermediate hosts. Though important, this relationship
obviously cannot explain spatial variation in the prevalence
of parasitic castrators that have only one host in their life
cycles. Other abiotic and biotic factors must play a role in
these species (Latham and Poulin, 2003). However, studies
of variation in prevalence of parasitic castrators with a
single host are uncommon (Alvarez et al., 2001; Korn et al.,
2005; Yamaguchi et al., 1994). Rhizocephalan barnacles
provide excellent models in which to investigate the
determinants of prevalence in such relatively simple
INTRODUCTION
Parasitic castrators cause the genetic death of their hosts; in
this sense, infection with such parasites is analogous to
being consumed by a predator (Kuris, 1974). In addition to
the obvious consequences for individual fitness, parasitic
castration can also have significant population-level
consequences. Unlike predation, which can increase the
fitness of remaining individuals by removing potential
competitors, parasitic castration creates nonbreeding individuals that may compete for limited resources with
members of their own species (Ritchie and Høeg, 1981;
Lafferty, 1993). In addition, males may waste reproductive
effort attempting to mate with parasitized females (Shields
and Wood, 1993). Because of their effects on fecundity,
models (Negovetich and Esch, 2008) and field observations
and experiments (Lafferty, 1993; Fredensborg et al., 2005)
suggest that parasitic castrators can reduce the density of
host populations and that the magnitude of this reduction is
largely a function of parasite prevalence (the proportion of
infected hosts in the population: Bush et al., 1997). The
prevalence of parasitic castrators in a population thus has
clear and strong effects on both average individual fitness
and population-level processes. Given these effects, understanding the causes of variation in prevalence in parasitic
castrators is an important goal in ecological parasitology.
Spatial variation in the prevalence of marine parasites is
driven, in part, by the same factors that drive variation in
the abundance and distribution of free-living benthic
marine organisms. These may include such things as
physical (Shanks and Wright, 1987; Roughgarden et al.,
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systems, as all rhizocephalans use only a single host during
their life cycles (Høeg and Lützen, 1995).
In this paper, we describe kilometer-scale spatial
variation in the prevalence of the rhizocephalan Lernaeodiscus porcellanae Müller, 1862, on its host porcelain crab
Petrolisthes cabrilloi Glasell, 1945. By morphology,
rhizocephalans are only recognizable as barnacles by two
of their larval forms, the nauplius and the cyprid. The adult
stage of the life cycle consists of the interna, an extremely
simplified system of root-like tissue that spreads throughout the host’s body and absorbs nutrients, and the externa,
the barnacle’s reproductive structure, which erupts from
under the abdomen of the host and takes the place of the
host’s own egg mass (Høeg and Lützen, 1995). A previous
study documented spatial variation in the prevalence,
defined as the proportion of collected crabs bearing
externae, of L. porcellanae in monthly samples of P.
cabrilloi at three sites near San Diego, California (Alvarez
et al., 2001). Alvarez et al. (2001) observed consistent
differences in prevalence among sites separated by only a
few km. Crabs collected from Bird Rock, for example, had
a mean prevalence of 35.2%, while the mean prevalence at
Dike Rock was consistently lower (9.7%). These sites are
separated by only 9 km. They offered no explanations for
the observed variation in prevalence among nearby sites.
In order to explore the causes of such variation we
carried out a study similar to that of Alvarez et al. (2001) at
four sites on the Palos Verde Peninsula, located in southern
California, about 30 km south of Los Angeles. Our first
goal was to see if our populations were like those described
by Alvarez et al. (2001) in the sense that they showed
substantial and consistent among-site variation in externa
prevalence. Having accomplished this, we investigated four
possible causes of this variation, listed below:
1) Externa prevalence is not a reliable proxy for ‘‘true’’
prevalence. As remarked earlier, Alvarez et al. (2001)
used externae as indicators of infection. However, it is
possible that the absence of externae is not a reliable
indicator of lack of infection; that is, crabs that lack
externae might still be infected, carrying only internae.
After initial infection of P. cabrilloi by L. porcellanae,
there is a period of approximately 3-4 months during
which the parasite is solely internal (Ritchie and Hoeg,
1981). Thus spatial (and temporal) variation in externa
prevalence might be explained, and smoothed over, by
such things as the recent history of infections in a
population, or barnacle reproductive effort, rather than
variation in true prevalence. We estimated true
prevalence in each population by estimating the
abundance of ‘‘cryptically’’ infected crabs (crabs
bearing internae but not externae) in both female and
male crabs and adding this to estimates of externa
prevalence.
2) Host susceptibility to infection varies among sites. If
hosts are infected with greater ease at one site over
another, this could explain higher rhizocephalan
prevalence at certain sites. Larvae of L. porcellanae
infect P. cabrilloi through their gills (Høeg, 1985) and
in turn P. cabrilloi defends itself from infection by
removing cyprid and kentrogon larvae from its gills
with special gill-cleaning appendages (Richie and
Høeg, 1981; Høeg et al., 2005; Rypien and Palmer,
2007). Healthy crabs are efficient at removing
practically all barnacle larvae; however, crabs with
lost or damaged gill-cleaning limbs, injured crabs, and
crabs that have just molted are incapable of ridding
themselves of all barnacle larvae (Høeg et al., 2005).
Spatial variation in appendage damage, because of
variation in predation intensity or damage from shifting
rocks, might explain among-site variation in prevalence; we thus measured the frequency of appendage
loss as a potential proxy for susceptibility to infection.
3) Prevalence varies between host sexes, and among-site
differences in sex ratio drive observed among-site
variation in prevalence. Female decapods often have a
higher prevalence of externae than males, a pattern
sometimes rationalized by the observation that the
pleons of females are often larger than those of males
and may protect the externa more completely (Høeg
and Lützen, 1995). To examine this possibility, we
compared prevalence among the sexes and the sex ratio
distribution of crabs at each site.
4) Prevalence varies with host age, and among-site
differences in host population age structure drive
observed among-site variation in prevalence. Positive
associations between host age and prevalence are often
observed in parasite populations (Guralnick et al.,
2004); this presumably arises because older hosts have
been exposed to infective stages for a greater length of
time than have younger hosts. Thus, variation in
externa prevalence may be due to variation in the age
structure of host populations. We assessed this
possibility by assuming that size structure was a good
proxy for age structure, and then comparing size class
distribution of crabs at each site with prevalence
among size classes.
MATERIALS AND METHODS
Field Collections
Petrolisthes cabrilloi were sampled approximately monthly at four
intertidal sites on the Palos Verdes Peninsula, California, U.S.A.: White
Point (33u429550N, 118u199090W), Trump Golf Course [hereinafter called
‘‘Trump’’] (33u439230N, 118u209120W), Point Vicente (33u449270N,
118u249140W), and Bluff Cove (33u479370N, 118u249250W) (Fig. 1).
Collections at White Point and Trump began in March, 2008, while
collections at the other two sites began in November, 2008. Collections
were conducted at all sites through May, 2009. All sites sampled each
month were visited within a few days of each other, on the same tide
series, with a few exceptions due to logistical constraints.
On each sampling date, 100 P. cabrilloi with a minimum carapace width
of 4 mm were collected by hand from under cobbles in the high intertidal
zone at each site sampled that day. Smaller crabs were excluded because
they were difficult to measure and sex accurately in the field, and because
preliminary observations suggested that rhizocephalan infections were
very rare in these crabs. At the site, we recorded the following information
for each crab: carapace width (measured with vernier calipers to the
nearest 0.1 mm); sex (based upon abdominal appendages); presence or
absence of a rhizocephalan externa; presence or absence of a crab brood
(for female crabs); presence or absence of mature ovaries (for female
crabs; if present, these could be seen ventrally as maroon tissue beneath
the cuticle of the pleon, near its juncture with the cephalothorax); and prior
damage to thoracic limbs, indicated by regenerating thoracic pereiopods.
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or a brood during the reproductive season then indicated lack of infection,
and the absence of ovaries or a brood served as an indirect indicator of
cryptic infection.
Estimates of cryptic parasitism in males and females produced similar
results. To produce a single estimate of true prevalence for each site and
sampling date, we used the estimates of the prevalence of cryptic
infections from males to correct estimates based solely on externa
prevalence. The estimated prevalence of male cryptic infection at a site
and sampling date was multiplied by the total number of crabs (both male
and female) that lacked externae in that sample. This yielded an estimate
of the prevalence of cryptically-infected crabs in that sample. This
estimate was added to the field estimate of externa prevalence to yield an
estimate of true prevalence.
For statistical analyses prevalence data was arcsine square-root
transformed. Exploratory analyses revealed that analyses of untransformed
data yielded very similar results in all cases.
RESULTS
Fig. 1. Map of the Palos Verdes Peninsula, California, showing the four
study sites.
Estimating True Prevalence
We used two methods to assess the possibility of cryptic infection having a
significant impact on prevalence measurements: searching for internae in
male crabs that lacked externae, and analysis of the frequency of
reproductively-active female crabs as a proxy for lack of infection. For
males, from each field sample of 100 P. cabrilloi, 25 males that lacked
externae were kept and maintained for up to a week in the laboratory in
recirculating seawater tanks at approximately 15uC. Crabs were then held
briefly at 220uC until movement stopped, dissected by removal of the
carapace, and inspected with a dissecting microscope for the presence of
internae. Dissections of ‘‘positive-control’’ crabs that bore externae
showed dense internae within the digestive gland, as shown for the
rhizocephalan Loxothylacus texanus Boschma, 1933 (Sherman et al.,
2008); therefore, we focused on the digestive glands when searching for
internae in crabs that lacked externae. The interna of L. porcellanae
consists of thin, branching rootlets, which are light yellow to white in
color. No internae were found until Auguest, 2008. Because we were not
sure whether samples taken before that date truly lacked internae, or we
had simply not recognized them, we omitted samples taken before August,
2008 from subsequent analyses.
Female crabs were not dissected. To make rough estimates of the
frequency of cryptic infection, we made the assumption that infected
females were immediately castrated once infected. The presence of ovaries
We collected a total of 4335 individuals of P. cabrilloi from
March, 2008 through May, 2009. Each month 100 crabs
were collected from each site, with the exception of August
(n 5 72) and September (n 5 96), 2008 at Trump and
April, 2009 at Bluff Cove (n 5 67). The overall externa
prevalences of L. porcellanae infecting P. cabrilloi at
White Point (n 5 1500), Trump (n 5 1468), Point Vicente
(n 5 700), and Bluff Cove (n 5 667) were 22.1% 6 9.3,
10.4% 6 4.7, 6.1% 6 2.2, and 4.6% 6 3.2, respectively
(mean 6 standard deviation).
Spatial Patterns in Externa Prevalence
Patterns in externa prevalence among sites and months are
shown in Figure 2 (with 95% confidence intervals
calculated as in Bush et al., 1997). Externa prevalence
varied among sites (two-way ANOVA of arcsine squareroot transformed data, F 5 17.48, P , 0.001), but not
among months (F 5 1.03, P 5 0.453). Differences in
prevalence among sites were primarily due to the high
prevalence at White Point relative to the other three sites
(Tukey post-hoc tests, P , 0.001 for all comparisons with
White Point). Though prevalence differences among the
Fig. 2. Monthly externa prevalence (with 95% confidence intervals) of Lernaeodiscus porcellanae on the porcelain crab Petrolisthes cabrilloi at the four
study sites. White Point and Trump were sampled from March, 2008 through May, 2009, and Point Vicente and Bluff Cove from November, 2008 through
May, 2009.
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obtained for males by dissection, was consistent among
sites and among months, which suggests that cryptic
infection could not account for the observed variation.
In all subsequent analyses we use externa prevalence as
an estimate of true prevalence, for our estimates of cryptic
parasitism are approximate for both males and females and
we lack good estimates of true prevalence for the first six
months of the study.
Limb Loss
Fig. 3. Monthly prevalence of Lernaeodiscus porcellanae parasitizing
Petrolisthes cabrilloi for August, 2008 through February, 2009 at four
sites. The bottom part of each bar indicates externa prevalence; the top part
of each bar represents an estimate of the magnitude of cryptic parasitism.
Each entire bar (both sections combined) represents an estimate of ‘‘true’’
prevalence. The asterisk (*) indicates a sample for which cryptic
parasitism was not quantified.
other three sites were not statistically significant, it is
interesting to note that the data for November, 2008
through May, 2009 (the dates on which all sites were
sampled) are suggestive of a latitudinal gradient in
prevalence, with the highest values observed in the south
(White Point) and the lowest in the north (Point Vicente
and Bluff Cove).
Estimates of True Prevalence
In samples taken during and after August, 2008, we
typically found one to three males per site that contained
internae in samples of 25 males that lacked externae.
Estimates of true prevalence based on male cryptic
parasitism are shown in Figure 3. On average, estimated
total prevalence was only slightly higher than externa
prevalence at each site, with average increases in
prevalence as follows: White Point (5.8%, averaged over
10 months), Trump (4.3%, 10 months), Point Vicente
(1.1%, 7 months), and Bluff Cove (4.6%, 7 months). Like
externa prevalence, estimated true prevalence varied
significantly among sites (two-way ANOVA of arcsine
square-root transformed data: F 5 12.39, P , 0.001), but
not among months (F 5 0.48, P 5 0.874). All significant
among-site differences were due to contrasts between
White Point and the other three sites (Tukey post-hoc tests,
P , 0.05 for all comparisons).
Over the course of this study we found no females that
bore externae and also carried broods or mature ovaries.
During the peak reproductive season of P. cabrilloi (March
through August at White Point and Trump, the two sites for
which we have data for an entire reproductive season), a
minimum of 85% of female crabs that lacked externae were
reproductively active. In March at Trump, and at both
Trump and White Point in August, all female crabs that
lacked externae were reproductively active. Thus, if our
assumptions are correct, a maximum of 15% of the female
crabs that lacked externae could possibly have been
cryptically infected. This value, which is similar to that
The frequency of crabs with re-growing appendages did not
vary among sites (one-way ANOVA of arcsine square-root
transformed data, F 5 0.42, P 5 0.74). At White Point,
Trump, Point Vicente, and Bluff Cove, the mean
percentages of crabs with at least one regenerating thoracic
limb were 7.7%, 7.4%, 8.9%, and 8.6%, respectively.
Host Sex Effects
There was a significant difference in sex ratio among all
sites (x2 5 12.701, d.f. 5 3, P 5 0.005), but when White
Point was excluded the sex ratio was the same for the other
three sites (x2 5 0.336, d.f. 5 2, P 5 0.846). White Point
had slightly more female crabs overall (713 males, 767
females), while the other sites had more male crabs (Trump
799 males, 672 females; Point Vicente 371 males, 328
females; Bluff Cove 355 males, 309 females). Numbers of
males and females at each site total to slightly less than the
total number of crabs sampled because it was difficult to
sex a few individuals at each site in the field. Externa
prevalence tended to be slightly higher in females than
males at all sites (White Point 19.6% males, 22.6%
females; Trump 8.6% males, 10.5% females; Point Vicente
5.6% males, 8.4% females; Bluff Cove 2.2% males, 3.5%
females). This difference was borne out by a paired t test
pooling data within sites and using the four sites as
replicates; this analysis showed that externa prevalence of
L. porcellanae was higher among females than among
males (paired t test of arcsine square-root transformed data,
t 5 8.248, d.f. 5 3, P 5 0.0037).
Host Age/Size Class Effects
All sites had similar crab size distributions except White
Point, where the population was strongly skewed toward
larger size classes (Fig. 4). The medians of monthly mean
carapace width were significantly different among the four
sites (Kruskal Wallis, H 5 31.82, P , 0.0001). All of these
differences were attributable to White Point (Dunn’s post
hoc multiple comparisons). Median crab carapace width at
White Point was significantly greater than at Trump (P ,
0.001) or Bluff Cove (P , 0.05), but not at Point Vicente.
Overall mean carapace width at White Point was 7.0 mm,
while mean carapace width at Trump was 5.6 mm, at Point
Vicente 6.1 mm, and at Bluff Cove 5.7 mm.
The prevalence of L. porcellanae increased with host
crab size (Fig. 5). Host size class explained 80.4% of the
overall variance in size-class specific prevalence (P ,
0.0001; slope 5 8.04, y-intercept 5 234.56; ordinary least
squares regression of prevalence versus host size class).
SLOAN ET AL.: PREVALENCE OF A RHIZOCEPHALAN BARNACLE
Fig. 4. Size-class distribution of Petrolisthes cabrilloi. For each site, data
were pooled across all months.
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DISCUSSION
Fig. 5. Externa prevalence within host size classes pooled across all
months for each of the four sites. Asterisks (*) indicate sample sizes of less
than 20, and zeroes indicate no crabs present in that size class at that site;
in both cases, estimates of prevalence should be viewed with caution.
The magnitude of the effect of parasitic castrators on host
populations is largely a function of parasite prevalence
(Lafferty, 1993; Fredensborg et al., 2005). The factors that
determine prevalence are diverse and often difficult to
distinguish. Rhizocephalans are parasites with relatively
simple life histories and serve as excellent models to
investigate the causes of variation in parasite prevalence. In
the San Diego region, Alvarez et al. (2001) documented
substantial variation in externa prevalence of L. porcellanae on the host decapod P. cabrilloi among nearby sites.
Our results for the same species at sites on the Palos Verde
Peninsula (located well to the north of San Diego) were
qualitatively similar to those of Alvarez et al. (2001). We
found striking and consistent differences in prevalence
among sites separated by just a few km. Like Alvarez et al.
(2001), we also noted substantial variation in prevalence
within sites among sampling times (Fig. 2). However, as
our sampling regime was not designed to identify temporal
variation in prevalence, we cannot exclude the possibility
that this temporal variation is simply due to chance, e.g.,
sampling error.
Although cryptically infected hosts are often ignored in
estimates of prevalence (Rainbow et al., 1979, Lützen, 1981),
we wanted to verify that true prevalence (not just its proxy,
externa prevalence) actually varied between sites before
investigating possible causes for variation in prevalence. Both
methods that we used to identify cryptically-infected crabs
(dissection of males to observe internae, and observation of
the frequency of castrated females during the reproductive
season) suggested that at all four sites very few P. cabrilloi
were cryptically infected. Thus, externa prevalence appears to
be a reasonable proxy for interna prevalence, and the observed
among-site differences in externa prevalence very likely
reflect variation in true prevalence.
In their study of the rhizocephalan Sacculina sp.
infecting the crab Hemigrapsus sanguineus (de Haan,
1835), Yamaguchi et al. (1994) identified by dissection
levels of cryptic parasitism similar to those we observed in
P. cabrilloi; at high prevalence sites (over 50%), 10.6% of
the true prevalence was accounted for by crabs that bore
only internae. In contrast, Werner (2001) used male
feminization as an indicator of interna presence, and by
this criterion estimated that , 30% of the Carcinus maenas
(Linnaeus, 1758) parasitized by Sacculina carcini Thompson, 1836 did not bear an externa. Thus the level of cryptic
infection may be species- or interaction-specific, and it is
important to test the reliability of externa prevalence as an
indicator of true prevalence in any study of prevalence in
rhizocephalans. This difference in prevalence is likely
influenced by the duration of the internal phase before the
externae emerge. Lernaeodiscus porcellanae has a relatively short internal phase (3-4 months) (Ritchie and Høeg,
1981). The internal phase of S. carcini is highly variable;
however, it is generally longer (up to three years),
especially in colder waters (Høeg and Lützen, 1995;
Lützen, 1984) like in Sweden where Werner’s (2001)
experiment took place.
One hypothesis that might explain the differences in
prevalence that we observed between White Point and the
other three sites is that there is spatial variation in host
susceptibility to infection. Susceptibility in P. cabrilloi may
vary for several reasons. First, P. cabrilloi uses its last pair
of thoracic appendages to reach into the gill chamber and
clean settling rhizocephalan cyprids off of its gills (Rypien
and Palmer, 2007). If these appendages are lost or
damaged, the frequency of successful infection increases
drastically (Ritchie and Høeg, 1981; Høeg et al., 2005).
Ritchie and Høeg (1981) found that P. cabrilloi collected
from mussel beds had lower rhizocephalan prevalences
than those collected from under cobbles, and suggested that
crabs that lived under cobbles were more subject to damage
by shifting rocks; loss of cleaning appendages at cobble
sites might thus lead to higher susceptibility to infective
cyprids. We measured the frequency of limb regeneration
at our sites as a proxy for ‘‘damage frequency,’’ but found
no differences among sites. Thus, our results do not support
the hypothesis that crab populations are differentially
susceptible to infection because of among-site variation
in limb damage.
Host susceptibility might also be related to among-site
variation in the frequency of ecdysis. Rhizocephalan
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cyprids can infect hosts more easily when the host is
molting and is less able to ward off cyprid settlement and
parasite invasion (Richie and Høeg, 1981; Høeg et al.,
2005). Thus, variation among sites in the total number of
molts experienced by crabs, which might be proportional to
crab age or the quality of the habitat, e.g., in terms of food
supply, might contribute to among-site variation in parasite
prevalence. We discuss this possibility further below.
The crab sex ratio at White Point was slightly femalebiased, but the ratio at the other three sites was slightly
male-biased. As in many previous studies, our results also
show that female hosts had a higher prevalence of
rhizocephalans than males. This is often ‘‘explained’’ by
the argument that female hosts have wider pleons that more
effectively protect the externae from damage (Høeg and
Lützen, 1995). The combination of a female-biased sex
ratio and a slightly higher prevalence of L. porcellanae in
female crabs undoubtedly contributes to the overall higher
rhizocephalan prevalence at White Point. However, this
effect cannot be very large, as ‘‘excess’’ prevalence in
females was less than or equal to only 3% at all sites.
The prevalence of L. porcellanae was much higher in
larger size classes of host crabs (Fig. 5), and the size
structure of the crab populations varied among sites in such
a way that host population size structure explained most of
the variation in prevalence among sites. Crabs at Trump,
Point Vicente, and Bluff Cove were small (Fig. 4) relative
to those at White Point, and therefore had relatively low
parasite prevalence. White Point, with much larger crabs,
had much higher parasite prevalence. The relationship of
host size class and prevalence explained 80.4% of the
overall variance in prevalence. Of all the potential
determinants of spatial variation in parasite prevalence
considered, size structure of the host population was clearly
the most important. Among-site variation in the size
structure of P. cabrilloi may have also contributed to the
similar pattern of spatial variation in prevalence observed
by Alvarez et al. (2001), but those workers did not report
size-frequency distributions for host crabs in their samples.
A previous study also found that the prevalence of L.
porcellanae in P. cabrilloi increased linearly with crab size
(Høeg and Lützen, 1995). This trend is different from some
other rhizocephalan systems where prevalence is higher in
small to medium hosts and lower in large hosts (O’Brien
and Van Wyk, 1985; Korn et al., 2005; Innocenti and Galil,
2007). These latter studies were conducted with rhizocephalans of the family Sacculinidae. Sacculinids typically
block host molting, either entirely, or at least when an
externa is present. In contrast, L. porcellanae does not
prevent P. cabrilloi from molting, even when an externa is
present (Høeg and Lützen, 1995). Size-class-specific
prevalence is influenced by a combination of when the
host can be infected, e.g., only at the molt that defines
reproductive maturity or throughout its entire life, and
whether or not it can molt (grow) once it is infected. For
example, if a rhizocephalan can only infect small crabs and
if the parasite prevents/slows host molting, then prevalence
is expected to be much higher in the smaller crabs. This is
the case in the sacculinid Sacculina carcini (Lützen, 1984;
Høeg and Lützen, 1995). In L. porcellanae, however,
prevalence is higher in larger host crabs (Høeg and Lützen,
1995; this study). As L. porcellanae does not prevent host
molting and growth, crab size is likely a reasonable proxy
for crab age; larger P. cabrilloi are presumably older and
have likely had lengthier exposure to L. porcellanae
propagules than have smaller crabs. Compounding this
simple effect of age is the effect of molting. Lernaeodiscus
porcellanae can infect P. cabrilloi with greater ease when
the crab is molting and cannot defend itself from cyprid
attack (Richie and Høeg, 1981). Even if they are not older,
larger crabs have likely gone through more molts than
smaller crabs and have thus been highly vulnerable to
rhizocephalan infection more often than smaller crabs.
This study revealed that the size distribution of the host
crab population may largely explain among-site variation in
rhizocephalan prevalence in southern California, and more
specifically, the relatively high prevalence of rhizocephalans at White Point. An obvious question arising from that
result is simply: why are crabs at White Point larger than at
the other sites? The most likely answers to that question are
that crabs at White Point are either older than crabs at other
sites, or that they grow more rapidly than crabs at other
sites. Crabs might live longer at White Point if there is
lower predation or more food available at that site. An
increased food supply at White Point might also lead to
more rapid growth of P. cabrilloi. Porcelain crabs are
primarily suspension feeders, and thus are largely dependent on the delivery of suspended food particles to the
intertidal zone by local productivity and water movements
(waves and currents). Local current patterns and upwelling
can cause kilometer-scale alongshore variation in particle
delivery to the intertidal zone (Bertness et al., 1991;
Menge, 1997). To ascertain whether more suspended food
is delivered to the intertidal zone at White Point compared
to nearby sites, future workers might compare growth rates
of other suspension feeders, e.g., Balanus glandula Darwin,
1854, among those sites.
Even in the absence of among-site variation in the
abundance of suspended food particles, it is possible that
crabs at White Point have access to more food than do crabs
at other sites. Gabaldon (1975) suggested that, in addition to
suspension feeding, P. cabrilloi can use tufts of flexible hairs
on its chelae to brush organic material from the substrate
towards its mouthparts. White Point may have an unusually
large amount of potential benthic food compared to the other
sites we studied. At White Point, shallow hydrothermal vents
in both the intertidal and the subtidal emit fluid high in
sulfide. This supports the growth of large populations of
sulfur-oxidizing bacteria that are available as food for some
benthic molluscs, at least (Stein, 1984; Kalanetra et al.,
2004). These bacteria may also serve as an additional food
source for P. cabrilloi at White Point, allowing them to grow
faster or live longer than crabs at other sites where suspension
feeding may be the only available feeding strategy. If this
suggestion is correct, then we would expect that other
southern California sites with intertidal hydrothermal vents,
e.g., Pt. Fermin on the Palos Verde Peninsula, to also have
larger porcelain crabs than sites that lack hydrothermal vents.
Finally, we should note that our observations of L.
porcellanae on the Palos Verde Peninsula represent a small
SLOAN ET AL.: PREVALENCE OF A RHIZOCEPHALAN BARNACLE
northward range extension for this rhizocephalan. Alvarez
et al. (2001) reported that the northern range limit of the
species was Laguna Beach, California; however, our
northernmost site (Bluff Cove) is , 90 shoreline km to
the north of Laguna Beach. If the Palos Verde Peninsula
actually does represent the northern range limit for L.
porcellanae, it is possible that some of the decline in
prevalence we observed at the northernmost sites is related
to the action of whatever physical or biological factors set
that boundary. Whether or not this hypothesis is plausible
can be resolved by estimating the prevalence of L.
porcellanae at sites north of the Palos Verde Peninsula;
its host crab reportedly occurs as far north as Morro Bay in
central California (Jensen, 1995).
ACKNOWLEDGEMENTS
We thank Drs. J. Archie and C. Whitcraft for statistical advice, and P.
Barillas, D. Schuessler, and K. Sloan for help in collecting and measuring
crabs. K. Anthony and C. Martin of the CSULB Marine Laboratory kindly
provided sea-table space in which to hold living specimens. We also thank
Dr. Mark Grygier and two anonymous reviewers for helpful comments on
an earlier version of the manuscript.
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RECEIVED: 24 June 2009.
ACCEPTED: 8 September 2009.