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Increased Parasitism of Limpets by a Trematode Metacercaria in Fisheries

Management Areas of Central Chile: Effects on Host Growth and Reproduction

Article  in  EcoHealth · October 2013

DOI: 10.1007/s10393-013-0876-9 · Source: PubMed

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EcoHealth
DOI: 10.1007/s10393-013-0876-9

Ó 2013 International Association for Ecology and Health

Original Contribution

Increased Parasitism of Limpets by a Trematode Metacercaria

in Fisheries Management Areas of Central Chile: Effects
on Host Growth and Reproduction

Management Areas and Parasitism

Marcela Aldana,1 José M. Pulgar,2 Nathalie Orellana,1 F. Patricio Ojeda,3

and M. Roberto Garcı́a-Huidobro1,2
1
Escuela de Pedagogı́a en Biologı́a y Ciencias, Facultad de Ciencias de la Educación, Universidad Central de Chile, Santa Isabel 1278, 6° piso, Santiago,
Chile
2
Departamento Ecologı́a y Biodiversidad, Facultad de Ecologı́a y Recursos Naturales, Universidad Andres Bello, República 470, Piso 3, Santiago, Chile
3
Departamento de Ecologı́a, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, Chile

Abstract: The rapid increase in body size and abundance of most species inside Management and Exploita-
tions Areas for Benthic Resources (MEABRs) has led to the proposal of these areas as a good complement for
achieving the conservation objectives of Marine Protected Areas (MPAs). However, when evaluating MEABRs
and MPAs as conservation and/or management tools, their impact upon parasite populations has rarely been
considered, despite the fact that epidemiological theory suggests an increased susceptibility to parasitism under
high population abundance. We evaluated the effects of MEABRs on the parasite abundance of Proctoeces
lintoni and its impact on the growth of the host limpet Fissurella crassa in central Chile. Parasitic magnitude
was higher inside MEABRs than in Open-Access Areas, and parasitized limpets showed a greater shell length,
muscular foot biomass, and gonadosomatic index compared to non-parasitized limpets of the same age. Our
results suggest that the life cycle of P. lintoni and, consequently, its trophic links have been strengthened inside
MEABRs. The increased growth rate could reduce the time required to reach the minimum catch size and
increase the reproductive and muscular output of the host population. Thus, parasitism should be considered
in the conservation and management of economically important mollusk hosts.

Keywords: human harvesting, rocky intertidal, Fissurella spp., MEABR, Proctoeces lintoni parasite, growth rings

INTRODUCTION tems (Moreno et al. 1984, Castilla and Durán 1985;

Numerous ecological studies have demonstrated the dra-
matic effects that humans have on coastal marine ecosys-
Correspondence to: Marcela Aldana, e-mail: maldanap@ucentral.cl
Moreno et al. 1986; Durán and Castilla 1989; Dayton et al.
1995; Castilla 1999; Pinnegar et al. 2000; Manrı́quez and
Castilla 2001; Shears and Babcock 2003). In Chile, as in
many other coasts of the world, top-down factors associ-
ated with the human exploitation of invertebrate, algae,
and fish play a major role in the regulation of local
Aldana et al.
intertidal communities, triggering a suite of direct and
indirect modifications in the structure and functioning of
rocky intertidal communities (Castilla et al. 1994; Castilla
1999). Marine Protected Areas (MPAs) have been created
as a means of fostering marine conservation (Dayton et al.
1995; Lubchenco et al. 1995; Allison et al. 1996) and have
provided an opportunity to study the long-term dynamics
of marine ecosystems (Castilla 1999, 2000).
Based on the knowledge acquired on ecosystem func-
tioning and the rate of replenishment of resources inside
MPAs, the government of Chile regulated access to eco-
nomically important benthic resources through the estab-
lishment of Management and Exploitation Areas for
Benthic Resources (MEABRs) in 1991 (Castilla et al. 1998;
Castilla and Fernández 1998; Castilla 1999, 2000). This
action has been proclaimed a management and economic
success due to the increase in benthic resource abundance
and body size inside MEABRs as compared to Open-Access
Areas (OAAs) (Castilla and Fernández 1998; Manrı́quez
and Castilla 2001; Gelcich et al. 2008; Guidetti and Claudet
2010). The muricid gastropod (Concholepas concholepas),
the sea urchin (Loxechinus albus), and three species of
keyhole limpets (Fissurella spp.) were larger in the El
Quisco MEABR than in open-access fishing grounds
(Castilla and Pino 1996; Castilla and Fernández 1998; Castilla
et al. 1998). Densities of C. concholepas and Fissurella spp.
were up to 15 times higher inside than outside the MEABRs
(Gelcich et al. 2008). Moreover, it has been suggested that
these areas provide important conservation add-on effects
for species that are not the focus of the management policies
(Gelcich et al. 2008; Guidetti and Claudet 2010).
Parasites represent an important component of eco-
systems whose biomass can exceed that of top predators
(Kuris et al. 2008), thus potentially playing a critical role in
conservation and sustainable management (May 1988;
Scott 1988; Lafferty and Gerber 2002). Basic epidemiolog-
ical theory predicts that the number of hosts in a popula-
tion influences the transmission success of parasites by
determining the contact rate between the parasites’ infec-
tive stages and the new hosts (Anderson and May 1979,
1991; Hudson et al. 2002). In addition, empirical evidence
suggests that host population density is indeed an impor-
tant predictor of both parasite abundance and parasite
species’ diversity (Arneberg et al. 1998; Morand and Poulin
1998; Bustnes et al. 2000; Loot et al. 2005; Aldana 2007). In
this context, the integration of basic epidemiological theory
and the effect of MEABRs on population abundance of
exploited species suggest that populations within these
areas would be more susceptible to parasitism (see
McCallum et al. 2005, Wood et al. 2010).
The impact that parasitic infections have on animal
populations in the wild has been recognized as an impor-
tant factor affecting the density and distribution of species
(Anderson 1979; Anderson and May 1979; Price 1980, see
Scott 1988 for a review). Parasites can play a key role in
structuring animal communities by influencing host mor-
tality, fecundity, growth, physiology, and behavior (Price
1980; Poulin and Thomas 1999; Sorensen and Minchella
2001; Lafferty et al. 2006), based on the differential sus-
ceptibility of the host species to infection and its conse-
quences (Price et al. 1986, 1988; Minchella and Scott 1991;
Thomas et al. 1995; Combes 1996; Bonsall and Hassel 1997;
Combes 1998; Hudson and Greenman 1998). However, it
has been more recently proposed that parasites could alter
traits that may not contribute to the disease process
(Thompson and Kavaliers 1994) and that they could like-
wise influence the host’s community structure (Thomas
et al. 2000; Miura et al. 2006; Miura and Chiba 2007; Byers
2009; Sonnenholzner et al. 2011), for example, by influ-
encing a host’s life history traits that are important deter-
minants of species coexistence in the host community
(Thomas et al. 2000). Thus, it has been suggested that
parasites can induce phenotypic alterations in their hosts
(Combes 1991; Poulin 1998; Thomas et al. 1998; Poulin
and Thomas 1999; Lafferty et al. 2000) which could inter-
fere with ecological and evolutionary processes relevant to
an ecosystem’s functioning (Thomas et al. 2000, 2006;
Ponton et al. 2005; Miura et al. 2006; Lefèvre et al. 2009).
In Chile, one of the host–parasite systems that has
received considerable attention involves the fellodistomid
trematode Proctoeces lintoni Siddiqi and Cable 1960 with its
intermediate host, the keyhole limpets Fissurella spp.
(Archaeogastropoda) (Bretos and Jirón 1980; Bretos et al.
1983; George-Nascimento and Quiroga 1983; Osorio et al.
1986; Oliva and Dı́az 1988, 1992; Oliva and Huaquin 2000;
Balboa et al. 2001; Ponciano 2001; Loot et al. 2005). A
three-host life cycle has been suggested for this parasite
(Oliva 1984; Oliva and Zegers 1988; George-Nascimento
et al. 1998; Balboa et al. 2001). It is thought that a mollusk,
specifically a mussel, acts as the first intermediate host in
which the parasite produces cercariae (see Aldana 2007).
These cercariae then leave the mussel to infect the gonads
of the keyhole limpet Fissurella spp., the second interme-
diate host, and where they develop into the metacercariae
stage. The infected limpet is then ingested by the definitive
host, the clingfish Syciases sanguineus, wherein the parasite

reaches sexual maturity. Through experimental protocols
and field studies in central Chile, Aldana et al. (2009)
suggested that the first intermediate host of P. lintoni would
be the mussel Perumytilus purpuratus. However, Oliva et al.
(2010) later refuted this idea by using molecular and
experimental evidence. Thus, the identity of the first
intermediate host is still debatable. In regard to keyhole
limpets, they are a diverse group of herbivores that inhabit
the mid–low intertidal and subtidal zone of the Chilean
coast (Castilla 1981; McLean 1984; Bretos 1988; Oliva and
Castilla 1992), and are among the most important prey
items collected by humans in central Chile (Durán et al.
1987; Bretos 1988; Oliva and Castilla 1986a, b; Pino and
Castilla 1995). Fissurella crassa is the most abundant species
in the mid–low rocky intertidal zone, and it presents the
greatest catch per unit effort among the keyhole limpets
caught by humans (Oliva and Castilla 1986a, b).
Fissurella spp. limpets are one of the main resources
whose extraction is regulated within MEABRs. There are
479 fully operational MEABRs, and approximately 61% of
these have limpet management policies (SERNAPESCA
2011). The MEABRs are spread over 1,100 km2 of the
Chilean coast, which exceeds the total area covered by five
no-take marine reserves, eight marine concessions with
conservation purposes, four multiple-use MPAs, and one
marine park (Fernández and Castilla 2005). Thus, the
MEABRs have the potential to scale-up the sustainable use
of benthic resources and also to enhance marine conser-
vation initiatives (Castilla 2000; Castilla et al. 2007; Daszak
et al. 2000; Gelcich et al. 2008). The purpose of this study
was to evaluate the effect that Management and Exploita-
tion Areas for Benthic Resources have on host–parasite
interactions. In particular, we focus on the magnitude and
effect of parasitism by the trematode P. lintoni on aspects
associated with the growth and reproduction of F. crassa.
We hypothesize increased infection rates in MEABRs
compared to OAAs, and therefore the potential effects of
the parasite on the host would be more important in
management areas.
METHODS
Study Sites
The sites we sampled on the central coast of Chile (Fig. 1)
correspond to three localities where the oldest MEABRs
were established: Quintay (33°100 S, 71°410 W) (*162 ha),
Parasitism of Limpets by a Trematode Metacercaria
El Quisco (33°230 S, 71°420 W) (*344 ha), and Las Cruces
(33°180 S, 71°380 W) (*85 ha). These MEABRs have been in
place for over 16 years and have been harvested as MEABRs
for over 15 years. At each locality, a site adjacent to the
MEABR was chosen as the OAA, where fishing and tourism
activities are common and harvesting of invertebrates from
the shore is intense and largely unregulated (Castilla and
Durán 1985; Castilla and Bustamante 1989; Durán and
Castilla 1989). At each locality, both the MEABR and OAA
selected sites were along approximately 500 m of coastline
and had similar geological characteristics, slope, wave
exposure, and tidal levels.
Host Abundance and Sampling
The abundance of F. crassa was quantified for the three
study sites along a 250-m horizontal transect located in the
lower–middle intertidal zone of each study locality. A
minimum of 20 and a maximum of 84 quadrants of
0.25 m2 were positioned at intervals of 2–3 m along each
transect. In each quadrant, the number of the Fissurella
crassa intertidal limpets was recorded. We collected speci-
mens of F. crassa manually from the intertidal zone at each
study site during the summer/autumn of 2010 (January–
May). From Quintay, we collected 210 specimens in the
MEABR and 226 specimens in the OAA. From El Quisco,
we collected 66 specimens in the MEABR and 31 specimens
in the OAA. From Las Cruces, we collected 81 specimens in
the MEABR and 35 specimens in the OAA. In all areas,
sectors with a low rocky slope (<45°) and semi-exposure
to waves were selected. All specimens were deposited in
plastic bags, labeled, and transported to the laboratory
where they were frozen (-20°C).
Magnitude of Parasitism
The magnitude of parasitism on F. crassa from the MEA-
BRs and OAAs at Quintay, El Quisco, and Las Cruces was
estimated by the prevalence, or percentage, of infected host
individuals and the parasitic intensity, or mean number, of
parasites per infected host (Margolis et al. 1982; Bush et al.
1997). In the laboratory, we estimated the soft body weight
of each limpet (no shell), and its gonad was isolated,
weighed, and sifted with water under high pressure. We
examined the material retained in a 0.5-mm mesh sieve
under a stereomicroscope, and counted and weighed all
specimens of P. lintoni.
Aldana et al.
Effects of Parasitism
The effects of the parasite on issues related to growth and
reproduction of F. crassa were estimated in specimens
collected from the locality that showed the greatest mag-
nitude of parasitism (Quintay). We measured the go-
nadosomatic index (gonad mass as a proportion of the
soft body mass), muscular foot biomass, and the length of
each growth ring as established and validated by Bretos
(1980) from parasitized and non-parasitized limpets. In
parasitized limpets, the parasite biomass was subtracted
from gonad biomass. The muscular foot biomass was
assessed in absolute terms as an estimator of limpet body
size without its shell. The muscular foot was used as this
structure represents the greatest volume of soft animal
biomass, serving as an important factor against wave
dislodgement (Serra et al. 2001; Pulgar et al. 2012), and as
it also corresponds to the organ commercialized by the
fishing industry (Osorio 2002). Additionally, we measured
the maximum shell length (shell edge) of parasitized and
non-parasitized limpets from the MEABRs and OAAs.
The number of growth rings was also recorded in order to
estimate limpet age (Bretos 1980), thus correcting for age
differences when comparing the shell edge or growth
rings’ lengths, muscular foot biomass, and gonadosomatic
index.
Figure 1. Locations of the three study
sites on the central coast of Chile where
limpets were collected. MEABR Man-
agement and Exploitation Areas for
Benthic Resources, OAA Open-Access
Area.
Statistical Analysis
The abundance of limpets and the magnitude of parasitism
were analyzed separately for each locality (Quintay, El
Quisco, and Las Cruces). Significant differences in the
abundance of the limpet F. crassa between areas (MEABR
and OAA) were evaluated by one-way analysis of variance
(ANOVA). We compared parasite prevalence between areas
and among ages (limpets with a different number of growth
rings) using a log-linear analysis on a 3-way contingency
table with G-square statistics (Fienberg 1977; Sokal and
Rohlf 1981; Zar 1999). We performed two-way ANOVA
to test for differences in parasite intensity in limpets be-
tween areas and among ages. These analyses were per-
formed on limpets with two, three, and four growth rings
at Quintay, and on limpets with two and three growth
rings at El Quisco and Las Cruces, as they were more
numerous. Area and age were considered as fixed factors
because our interest was focused on the differences within
and outside MEABRs and among proposed ages, and the
conclusions are limited at these levels (Bennington and
Thayne 1994). We used a Tukey post-hoc test to analyze
the statistical significance between groups (Sokal and
Rohlf 1981; Zar 1999).
To evaluate the effect of the parasite on F. crassa
growth while considering the age of the limpets, the growth

rings and shell edge lengths were analyzed using repeated
measures ANOVA, where main effects were the parasitism
condition and growth ring, with repeated measures on
growth ring or shell edge lengths. This analysis was per-
formed with limpets of three growth rings as they were
more numerous. Furthermore, we compared the maximum
shell length (shell edge) between MEABRs and OAAs,
considering parasitism, by two-way ANOVA.
We also performed a two-way ANOVA to compare the
muscular foot biomass and gonadosomatic index between
parasitized and non-parasitized limpets of different ages as
fixed factors. We used a Tukey post-hoc test to analyze the
statistical significance between groups (Sokal and Rohlf
1981; Zar 1999).
RESULTS
Host Abundance
In Quintay and Las Cruces, the abundance of F. crassa
limpets varied significantly between areas (Quintay:
F1,122 = 4.43, P = 0.037; Las Cruces: F1,88 = 7.67,
P = 0.007), with a greater abundance in MEABRs than in
OAAs. In contrast, in El Quisco, the abundance of keyhole
limpets did not show significant differences between areas
(F1,130 = 2.10, P = 0.150; Fig. 2).
Magnitude of Parasitism
In all localities, the prevalence of P. lintoni in F. crassa limpets
of the same age (number of growth rings) varied significantly
between areas (MEABR and OAA) (Quintay: G 2(3) = 230.02,
P < 0.0001; El Quisco: G 2(2) = 7.54, P = 0.023; Las Cruces:
G 2(2) = 29.26, P < 0.0001). In Quintay and Las Cruces, the
Figure 2. Average abundance of limpets Fissurella crassa in the
Management and Exploitation Area for Benthic Resources (MEABR)
and Open-Access Area (OAA) at Quintay, El Quisco, and Las Cruces.
Bar indicates ± 1 standard error. Asterisk Indicates significant
differences between areas.
Parasitism of Limpets by a Trematode Metacercaria
quantity of parasitized limpets observed inside the MEABRs
was significantly higher than at the OAAs (Fig. 3), while the
opposite was observed in El Quisco (Fig. 3).
Similarly, in both Quintay and Las Cruces, the mean
parasite intensity observed at the MEABR was significantly
higher than that observed at the OAA after considering the
age of the limpet (Quintay: F1,181 = 29.61, P < 0,0001; Las
Cruces: F1,67 = 198.44, P = 0,0395; Fig. 4). In contrast, for
El Quisco, the result depends on the number of growth
rings (F1,51 = 4.54, P = 0.038; Fig. 4). The parasitic load
observed in limpets with three growth rings for this locality
was greater in the OAA than in the MEABR (Tukey test,
P = 0,008), with no significant differences in limpets of two
growth rings (Tukey test, P = 0,397) (Fig. 4).
Effects of Parasitism on Host Growth
For limpets with three growth rings, beginning from the
second ring, the ring length observed in parasitized limpets
was significantly higher than that observed in non-para-
sitized ones (F3,465 = 6.66, P < 0.0001; Fig. 5). When the
Figure 3. Percentage of parasitized Fissurella crassa with a different
number of growth rings in the Management and Exploitation Area
for Benthic Resources (MEABR) and Open-Access Area (OAA) at
Quintay, El Quisco, and Las Cruces.
Aldana et al.

Figure 4. Parasite intensity of Proctoeces lintoni on Fissurella crassa with a different number of growth rings in the Management and
Exploitation Area for Benthic Resources (MEABR) and Open-Access Area (OAA) at Quintay, El Quisco, and Las Cruces.

condition of parasitism (parasitized or non-parasitized)

was considered, no significant differences of maximum
shell length were observed between MEABRs and OAAs
(Quintay: F1,432 = 0.03, P = 0.870; El Quisco: F1,93 = 2.40,
P = 0.125; Las Cruces: F1,112 = 4.02, P = 0.050; Fig. 6). For
both the MEABRs and OAAs, the maximum shell length
observed in parasitized limpets was significantly higher
than that observed in non-parasitized limpets (Quintay:
F1,432 = 72.08, P < 0.001; El Quisco: F1,93 = 4.32,
P = 0.040; Las Cruces: F1,112 = 15.73, P < 0.001; Fig. 6).
Finally, in the three most abundant age classes of
limpets (two, three, and four growth rings), the muscular
foot biomass and gonadosomatic index of parasitized
limpets were significantly higher than that observed in non-
parasitized limpets, independent of age (Muscular foot
biomass: F1,356 = 67.37, P < 0.001; Fig. 7. Gonadosomatic
index: F1,353 = 59.98, P < 0.001; Fig. 8).
DISCUSSION
Management and Exploitation Areas represent one of the
most promising management tools for sustainable exploi-
Figure 5. Average length of the growth ring and shell edge in
parasitized and non-parasitized Fissurella crassa of three growth rings
at Quintay. Bar indicates ± 1 standard error. Significant differences
in means between parasitized and non-parasitized limpets are
indicated with an asterisk.
tation of nearshore marine benthic resources (Fernández
and Castilla 1997; Castilla and Fernández 1998; Castilla
et al. 1998; Castilla 2000; Manrı́quez and Castilla 2001). In
addition, recent studies indicate that this management tool
provides important conservation add-on effects for species
that are not the focus of the management policies and
could complement the biodiversity objectives of fully pro-
tected areas (such as no-take MPAs) (Gelcich et al. 2008;
Guidetti and Claudet 2010). Overall, our results support

Figure 6. Average shell length of parasitized and non-parasitized
Fissurella crassa inside of Management and Exploitation Areas for
Benthic Resources (MEABRs) and in Open-Access Areas (OAAs) at
Quintay, El Quisco, and Las Cruces. For each locality, total average
shell length independent of the parasitism condition is also indicated.
Bar indicates ± 1 standard error. Significant differences in means
between parasitized and non-parasitized limpets are indicated with
an asterisk.
Figure 7. Average muscular foot biomass of parasitized and non-
parasitized Fissurella crassa with two, three, and four growth rings at
Quintay. Bar indicates ± 1 standard error. Significantly different
means between parasitized and non-parasitized limpets are indicated
with an asterisk.
that conditions generated by harvesting regulations on
coastal communities within MEABRs not only promote an
increase in the abundance of limpets (Fig. 2) but also
facilitate the dynamics of embedded parasite populations. In
Parasitism of Limpets by a Trematode Metacercaria
two of the three sites studied, the parasitism of the keyhole
limpet F. crassa by the trematode P. lintoni was significantly
higher in the MEABR than in OAA. This outcome was not
associated with parasite accumulation with host age, but
with a significant change in parasite population dynamics,
since even limpet individuals of the same age have greater
parasitism in MEABRs than in OAAs (Figs. 3, 4).
The biological nature of parasitism incorporates nat-
ural characteristics that are informative and useful for
management and conservation (Marcogliese 2001, 2005;
Huspeni et al. 2005). Trematodes are particularly useful
ecological indicators because they require multiple hosts
(invertebrate and vertebrate) to complete their life cycles,
and their transmission often relies on predator–prey
interactions. Consequently, the assemblage of trematodes
within a host organism potentially reflects the host’s tro-
phic position within the food web as well as the presence of
any other organisms that participate in the various para-
sites’ life cycles in the ecosystem (Marcogliese and Cone
1997; Marcogliese 2002, 2003; Hechinger and Lafferty 2005;
Huspeni et al. 2005; Hudson et al. 2006; Hechinger et al.
2008). In this sense, the higher prevalence and intensity of
the trematode P. lintoni in limpets from MEABRs as
compared to limpets of OAAs (Figs. 3, 4), in two of the
three sites evaluated, suggest that the life cycle of the par-
asite and consequently its trophic links are strengthened
inside of management areas.
The non-significant differences in the parasite abun-
dance at El Quisco could be associated with the limited
geographical size of the MEABR at this locality (57 hect-
ares, compared to 162 and 84 hectares at Quintay and Las
Cruces, respectively) as it is possible that the parasite dis-
persion area exceeds the MEABR’s limits. Moreover, the
higher level of parasitism in the first intermediate host
mussels and second intermediate host limpets in protected
areas compared to exploited areas has been attributed to
higher densities of the definitive host Sicyases sanguineus
(Loot et al. 2005; Hechinger et al. 2008). Thus, a small
protected area may be less important on the mobile
clingfish density, which would result in similar parasite
abundance. On the other hand, an alternative explanation
might consider that differences in parasite abundance could
be related to external aspects not associated with the
management area, such as environmental factors affecting
the biology of the host–parasite system. If so, the nearest
localities (Quintay and El Quisco, or El Quisco and Las
Cruces) would be expected to present a similar abundance
pattern, which was not observed.
Aldana et al.
Figure 8. Average gonadosomatic index of parasitized and non-
parasitized Fissurella crassa with two, three, and four growth rings at
Quintay. Bar indicates ± 1 standard error. Significant differences in
means between parasitized and non-parasitized limpets are indicated
with an asterisk.
As in the present study, Loot et al. (2005) also reported
increased levels of parasitism on keyhole limpets from
MPAs; however, in their analysis, both a marine reserve (no-
take MPA) and a MEABR were considered as MPAs. Our
study addresses only MEABRs and shows that the magnitude
of parasitism observed within these areas is about three times
higher than in OAAs (Figs. 3, 4), suggesting an increase of
host taxa that are part of the P. lintoni life cycle (i.e., mussels,
keyhole limpets, and clingfish) (Oliva and Zegers 1988;
George-Nascimento et al. 1998; Loot et al. 2005; Aldana et al.
2009; Valdivia et al. 2010). Consequently, our results are
consistent with studies that attribute MEABRs with signifi-
cant effects on the conservation of not only economically
important benthic invertebrates but also of species that are
not the focus of management policies (Gelcich et al. 2008).
However, the lack of replication due to logistical constraints
(only three MEABRs were examined) leads us to interpret
the probability values with caution, and we cannot statisti-
cally determine if the management areas and open-access
areas differ in parasite abundance on limpets solely based on
different fishing and extraction regulations.
By definition, any parasite will damage its host to a
certain degree, with effects ranging from minor metabolic
changes to severe tissue destruction (Lauckner 1980, 1983;
Price 1980). In the intertidal zone, trematode infection
affects a wide range of traits associated with survival,
reproduction, growth, and behavior of their hosts (see
Mouritsen and Poulin 2002 for a review). More specifically,
it is reported that the well-developed acetabulum of
unencysted P. lintoni can exert severe mechanical damage
on the structure and function of the limpet’s gonad (Oliva
1992; Oliva and Vega 1994; Oliva and Vásquez 1999).
However, Loot et al. (2005) found no serious detrimental
effect associated with increased parasite load on limpets
from protected areas in central Chile. Even more surpris-
ingly, our results suggest that P. lintoni markedly alters host
body size and reproductive output, with infected limpets
showing greater shell length, muscular foot biomass, and
gonadosomatic index when compared to non-parasitized
limpets of the same age (Figs. 5, 6).
Fissurella crassa has been described as a mainly inter-
tidal species that is not a part of the usual diet for the
clingfish Syciases sanguineus because of mouth width
restrictions of small intertidal clingfish and because of the
consumption of other keyhole limpet species by large,
subtidal clingfish (Castilla and Cancino 1988; Muñoz and
Zamora 2011; unpublished data). Thus, P. lintoni specimens
parasitizing F. crassa have been considered unencysted
progenetic metacercariae with a precocious development,
which would facilitate the transmission of this parasite
species in intertidal conditions where there is a low proba-
bility of consumption by a definitive clingfish host (Oliva
and Huaquin 2000; Aldana 2007; Oliva and Alvarez 2011).
McCarthy et al. (2004) suggest that increased host growth
may be favored in parasites with abbreviated life cycles and
when host viability increases parasite transmission. The
increase in body size of parasitized limpets could mean a
better body condition that contributes to the survival of
F. crassa. In this sense, the foot of F. crassa appears to be an
important attribute against the risk of wave dislodgement
(Serra et al. 2001; Pulgar et al. 2012), so a greater develop-
ment of the muscular foot could increase the lifetime of the
limpet. In this context, an increase in the survival of the host
may be beneficial not only to the host but also for parasite
reproduction and/or transmission.
In addition, the effect of the parasite on limpet growth,
as described above, apparently serves to increase the
available volume for parasite biomass (McCarthy et al.
2004), so that the increase in gonadal biomass would
provide more space for the accumulation of greater num-
bers of progenetic metacercariae (our data indicate that
infection intensity reaches 108 parasites), especially when
the parasite presents an extended residence in the gonads of
Fissurella spp. (George-Nascimento et al. 1998). Alterna-
tively, the enlargement of the gonad could mean a decrease
in the function of this organ, which would be consistent
with the structural and functional disorganization of the
gonad reported for F. crassa in northern Chile (Oliva 1992;
Oliva and Vega 1994; Oliva and Vásquez 1999).
Given the greater body growth (i.e., shell length and
muscular foot biomass) and gonadosomatic index of in-
fected limpets compared to non-parasitized limpets of the

same age, the incidence of P. lintoni in the F. crassa pop-
ulation may have important implications for the energy
budget and population dynamics of the host. First, the
increased growth and reproduction of the parasitized host
is physiologically constrained by the amount of resources
an individual has at its disposal; as more resources are
devoted to reproduction, fewer will be available to maintain
growth or survival. However, individuals can allocate re-
sources to two or more traits to the extent that it can
consume sufficient resources (Agnew et al. 2000). There-
fore, parasitized keyhole limpets may increase their rate of
food consumption in comparison with individuals non-
parasitized. Secondly, the parasite could affect the size
structure of the limpet population, both inside and outside
MEABRs. While the body size of limpets in management
areas is larger than those outside, when considering the
condition of parasitism, such differences become irrelevant
(Fig. 6). Thus, the larger body size of limpets within
MEABRs could rather be attributed to an increase in par-
asite load and the positive effect of parasites on the growth
of keyhole limpets. Therefore, our results suggest that a
high level of parasitism in management areas could be an
important factor in the increased body size of mollusks
observed within these areas (Castilla and Fernández 1998).
These aspects represent interesting and relevant issues for
future research.
From a fishery management perspective, our results
suggest that parasites can help reduce the required time to
reach the minimum catch size. Chile’s fishery legislation
indicates that the minimum size capture for the resource
Fissurella spp. is 65-mm shell length (Resolución 248/1996,
Ministerio de Economı́a, Fomento y Reconstrucción).
Bretos (1980) indicated that the F. crassa limpets form two
growth rings per year, usually during the summer and
winter. Thus, our data suggest that the parasitized keyhole
limpets achieve a minimum capture size at least a year
earlier than non-parasitized limpets (Fig. 6). Additionally,
the muscular foot biomass, an organ processed and com-
mercialized by the fishing industry (Osorio 2002), is about
three times higher in parasitized limpets than non-para-
sitized ones of the same age (Fig. 7). Therefore, trematode
parasitism might be relevant for the conservation and
management of economically important mollusk hosts.
However, an analysis of features that can reduce the mar-
ketability of the resource (e.g., muscular tissue consistency
and organoleptic traits of parasitized and non-parasitized
F. crassa) and of the long-term persistence of the host
population (e.g., limpet eggs viability) is needed to unravel
Parasitism of Limpets by a Trematode Metacercaria
the meaning of the parasite’s effects on the limpet popula-
tion. In addition, and in order to verify the importance and
generality of our findings, it will be necessary to assess the
magnitude and impact of parasites on other limpet species
(e.g., F. maxima and F. cumingi) also subjected to intense
human exploitation. It is likewise necessary to carry out
further evaluations on management areas in other regions of
the country, e.g., the north, where parasites have been re-
ported to have a negative effect on keyhole limpets (Oliva
1992; Oliva and Vega 1994; Oliva and Vásquez 1999).
ACKNOWLEDGMENTS
This study was funded by the internal grants of the
Universidad Central de Chile to Marcela Aldana, DI-02-
11/I Universidad Andres Bello to M. Roberto Garcı́a-
Huidobro, and DI 17-10/R Universidad Andres Bello to José
M. Pulgar. This study was conducted in fulfillment of the
Conservation Medicine PhD degree by MR G-H, Univers-
idad Andres Bello. We thank Paula Plaza and Cristian
Guerrero for help in the field, fishers at Caleta El Quisco, Las
Cruces, and Quintay for their support, and two anonymous
referees for useful comments on an earlier draft.
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