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The selective advantage of host feminization: A case study of the green crab Carcinus maenas and the parasitic barnacle Sacculina carcini


Abstract and Figures

Male crabs infected by parasitic barnacles (Rhizocephala) are known to be morphologically feminized. Here, we investigate morphological chances in green crabs, Carcinus maenas, induced by the parasitic barnacle Sacculina carcini. Infected males acquire a broader, longer and segmented abdomen, fringed with marginal setae. Copulatory appendages and pereopods are reduced in length, and the chelae become smaller. The feminization show great individual variation. Males with scars from lost externae, the parasites reproductive organ situated under the abdomen, are less modified than males carrying an externa, and the feminization is more pronounced in smaller than in larger males. No super-feminization is evident in female crabs that remain morphologically unaffected by infection. The protective value of a parasitically induced enlargement of the male abdomen may constitute an adaptation that increases parasite longevity. The additional effects on male morphology are viewed as pleiotropic side effects of the main adaptive value of enlarging the abdomen.
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The selective advantage of host feminization: a case study
of the green crab Carcinus maenas and the parasitic
barnacle Sacculina carcini
Tommy Kristensen Anders Isberg Nielsen Anders Isak Jørgensen
Kim N. Mouritsen Henrik Glenner Jens T. Christensen Jørgen Lu
Jens T. Høeg
Received: 13 April 2012 / Accepted: 19 June 2012 / Published online: 5 July 2012
ÓSpringer-Verlag 2012
Abstract Male crabs infected by parasitic barnacles
(Rhizocephala) are known to be morphologically femi-
nized. Here, we investigate morphological chances in green
crabs, Carcinus maenas, induced by the parasitic barnacle
Sacculina carcini. Infected males acquire a broader, longer
and segmented abdomen, fringed with marginal setae.
Copulatory appendages and pereopods are reduced in
length, and the chelae become smaller. The feminization
show great individual variation. Males with scars from lost
externae, the parasites reproductive organ situated under
the abdomen, are less modified than males carrying an
externa, and the feminization is more pronounced in
smaller than in larger males. No super-feminization is
evident in female crabs that remain morphologically
unaffected by infection. The protective value of a parasit-
ically induced enlargement of the male abdomen may
constitute an adaptation that increases parasite longevity.
The additional effects on male morphology are viewed as
pleiotropic side effects of the main adaptive value of
enlarging the abdomen.
The way rhizocephalan barnacles influence their crusta-
cean hosts has elicited considerable interest, since Giard
(1886) discovered that males of the spider crab Macro-
podia rostrata L., 1758, parasitized by the sacculinid
Drepanorchis neglecta Fraisse, 1877, adopted a number of
feminine traits, in particular a broadened abdomen. In
female crabs, the abdomen covers and protects the egg
mass of the gravid crab and, if parasitized by D. neglecta,
the external reproductive apparatus, the externa, of the
parasite. Male crabs have narrow abdomens that fit in a
groove of the thoracic sternum of the crab like a key in a
lock. Infected male crabs develop abdomens as broad as
females that provide the same degree of protection to the
parasite as is normally offered to the brood. Since Giard’s
discovery, it has become clear that all studied brachyuran
hosts parasitized by species of the family Sacculinidae
become morphologically modified, sterilized and sub-
jected to physiological and behavioural changes (Høeg
and Lu
¨tzen 1996; Høeg 1996). As a rule, males are much
more heavily influenced than females and may be femi-
nized to such a degree that on a superficial view they
become almost indistinguishable from the opposite sex. In
most cases, sacculinized females undergo no morpholog-
ical changes.
Sacculina carcini Thompson, 1836, parasitizes a great
number of portunid crab species (Høeg and Lu
¨tzen 1985;
Øksnebjerg, 2000). There are several reports on how it
influences its host morphologically, but some of them
pertain to another species of Sacculina,S. benedeni
Kossmann, 1872 (Bulgurkov 1938; Vernet-Cornubert
1958). Day (1935) studied the way S. carcini influences
Liocarcinus holsatus (Fabricius, 1798) while Veillet
(1945) examined the modifications inflicted by S. carcini
Communicated by S. A. Poulet.
T. Kristensen J. Lu
¨tzen J. T. Høeg
Department of Biology, Section for Marine Biology,
Copenhagen University, Universitetsparken 4,
2100 Copenhagen, Denmark
A. I. Nielsen A. I. Jørgensen K. N. Mouritsen (&)
J. T. Christensen
Department of Bioscience, Marine Ecology, Aarhus University,
Ole Worms Alle
´1, 8000 Aarhus C, Denmark
H. Glenner
Department of Biology, Biological Institute, University
of Bergen, Thormøhlsgae 55, 5020 Bergen, Norway
Mar Biol (2012) 159:2015–2023
DOI 10.1007/s00227-012-1988-4
on the estuary crab, Carcinus aestuarii Nardo, 1847. From
these studies, it is apparent that the degree each individual
S. carcini parasite exerts on its host is much more variable
than the non-or-all effect observed in D. neglecta.This
applies in particularly to how S. carcini modifies its
classical host, the green crab Carcinus maenas, where the
abdominal morphology of an infected male crab ranges
from almost no modifications to an appearance approxi-
mating that of an adult female (present study). This var-
iation of a parasite-induced host character of potential
importance for the survival of the parasite provides an
excellent chance for studying a morphological trait under
possible Darwinian selection. Hence, as part of a 3-year
study of the biology and parasites of the green crab, we
embarked on a large-scale field study on how C. maenas
is morphologically affected by S. carcini. In particular, it
was decided to investigate to what extent a feminized host
abdomen is of selective advantage for the parasite.
Materials and methods
Field sampling and measurements
In total, 366 uninfected and 249 sacculinized green crabs
were included in the study, all collected at four localities
in Limfjorden, Denmark. Limfjorden is a major but
shallow waterway (depth typically 4–6 m) that traverses
the northern part of Jutland connecting the North Sea
with the Kattegat/Baltic Sea estuary. The salinity varies
from c. 31 psu in the west to c. 23 psu in the east, with
bottom temperatures between 18 °C in July–August and
1–2 °C in February–March. The green crabs occur at all
depths and all over the fjord, while S. carcini in some
years may be absent from some of the eastern less saline
Crabs were caught in baited traps at three localities:
Venø Bay, off Bjørndrup and Lovns Broad (May–August
2009; depths: 1–6 m; salinity: 28–31 psu, 22–29 psu and
22–25 psu, respectively). Crabs from a fourth locality, off
Rønbjerg harbour, were collected in fish traps (26 June–2
July 2006; 2 m; 26 psu). The majority of the crabs was
above 30 mm in carapace width and therefore considered
mature. Six types of crabs were distinguished: apparently
non-parasitized males and females, parasitized males and
females with externae of Sacculina carcini, and parasitized
male and female crabs with scars from externae that had
been lost. Only few sacculinized female crabs were caught
at Rønbjerg, and thus, the analyses of these data focus
solely on males and non-infected females. The abdomens
of all crabs were lifted from the thorax to inspect them for
infestation (presence of externa or scar). To verify that all
apparently non-infected crabs were indeed uninfected, the
crabs from Lovns Broad, Venø Bay and Bjørndrup were
dissected for presence of an internal root system. The non-
infected crabs used for comparison were chosen randomly,
and damaged specimens were discarded. The number and
infection status of crabs used in the study are found in
Table 1. Besides the externally sacculinized crabs, a
number of males with broader abdomens than usual were
found. When dissected, those crabs were found to contain
rhizocephalan rootlets. Such crabs were also noted by Day
(1935), who explained them as sacculinized males that had
lost their externae and moulted again, and by Werner
(2001), who considered them parasitized males, the externa
of which had not yet emerged. In the present study, these
males were excluded from the analysis.
The following characters were measured on the col-
lected green crabs: (1) carapace width (CW) defined as the
distance between the fifth pair of lateral spines (Fig. 1a);
(2) maximum width of abdominal segment 3, 5 and 6
(Fig. 1b–d); (3) maximum length of abdominal segment 6
(Fig. 1b–d); (4) distance from base to tip of the left first
pair of pleopod of males (copulatory appendage) (Fig. 1f);
(5) height of the right claw from the dorsal notch near the
base of movable finger to the ventral margin (Fig. 1g); (6)
length of left and right pereopod 3 (second walking leg)
from base to tip (Fig. 1h). Data from solely the longer of
the two measured pereopods were used in the analysis.
Carapace width and pereopod length were measured by
ruler to the nearest mm, whereas the remaining characters
were measured to the nearest 0.1 mm using a dissection
Table 1 The total material studied distributed on sampling location and gender of the host, green crab Carcinus maenas
Location Males Females
Uninfected With externa With scar Uninfected With externa With scar
Lovns Broad (56°380400N,9°130300E) 49 0 0 0 0 0
Bjørndrup (56°4902500N,8°5104100E) 0 17 16 2 13 0
Venø Bay (56°3402800N,8°4003900E)0542988342
Rønbjerg (56°5302800N,9°904900E) 118 84 0 109 0 0
Uninfected: non-sacculinized crabs; with externa: sacculinized crabs possessing an externa; with scar: sacculinized or previously sacculinized
crabs with scar after lost externa
2016 Mar Biol (2012) 159:2015–2023
microscope fitted with an ocular micrometer. Pereopod
length, width of the fifth abdominal segment and length of
segment 6 were only obtained from crabs collected at
Rønbjerg, on which animals no measure of abdominal
segment 3 and claw height was achieved.
Morphological modification as a result of sacculiniza-
tion is expressed as the relative abdominal width (RAW),
defined as the ratio between the widths of segment 3
(which is comparatively unaffected) and segment 6 (which
increases following infection). This measure could not be
calculated for the Rønbjerg sample, and hence, the width of
segment 6 is expressed in relation to CW. Also, length of
the copulatory appendage, claw height and length of the
second walking leg are expressed in relation to CW.
Explanation of terms: externa—the bean-shaped repro-
ductive body of the rhizocephalan parasite attached to and
located under the ventral side of the crab’s abdomen.
Scar—a dark, circular spot arising from the point of
attachment when the externa had died and detached.
Scarred crabs—crabs with a scar. Sacculinized crabs—
crabs infected by S. carcini.Externally sacculinized
crabs—crabs having a visible externa or scar. Root sys-
tem—the sacculated trophic part of the parasite that
consists of numerous connected tubular and semitranspar-
ent rootlets embedded in the host tissue.
Data analyses
The data analysis was carried out using IBM SPSS 19.0
(one-way analyses) and SMATR 2.0 (regressions and
ANCOVA). In those instances where data did not meet the
prerequisites of parametric tests (normality, homogeneity
of variance), data were either transformed prior to analysis
or nonparametric tests were applied. All performed post
hoc tests are corrected for multiple comparisons.
Crabs from Rønbjerg were analysed separately by
expressing all measured characters as a function of CW in
analyses of covariance comparing the three main groups of
crabs in question: infected males, uninfected males and
uninfected females. This was done because the Rønbjerg
animals (1) were collected at a single site within a narrow
time span and depth (low variance), (2) included a rela-
tively large number of individuals from all of the three
main crab groups (see Table 1) (high statistical power) and
(3) were not measured for the width of segment 3 (inval-
idating RAW calculation, and hence, one-way analyses).
Fig. 1 Morphological characters and measures taken on uninfected
and sacculinized green crabs Carcinus maenas.aDorsal view of
carapace. Dorsal view of abdomen of non-infected female (b) infected
male with marginal setae (c) and non-infected male (d). eVentral
view of infected but unmodified male with scar from lost externa
(white arrow). fCopulatory appendage (pleopod 1). gClaw. hPereo-
pod 3 (second walking leg). The double-arrows show distances
measured. Not to scale; see text for details
Mar Biol (2012) 159:2015–2023 2017
Abdominal morphology
The relative abdominal width (RAW) of crabs from Venø
Bay, Bjørndrup and Lovns Broad combined, differed
according to infection status and gender (Fig. 2a). The
RAW of externally sacculinized males (externae present)
was significantly smaller (i.e. having broader abdomen; on
average 11.1 %) than that of uninfected males (Fig. 1c–d),
whereas scarred sacculinized males (Fig. 1e) attained
intermediate RAW values. In an analysis including also
female categories, scarred males were statistically similar
to the remaining male categories (Fig. 2a). Considering
solely males in a separate analysis, all three male catego-
ries could be separated statistically (Kruskal–Wallis test,
=65.73, P\0.0005; post hoc test: P[[\0.0005;
0.044]). Hence, scarred males have a slightly narrower
abdomen than males with externae, but also a broader
abdomen than non-infected males. Females on the other
hand attained a similar RAW regardless of infection status
and always had a broader abdomen than any male
(Fig. 2a). For all three male categories, there was no sig-
nificant relationship between RAW and carapace width
(Linear regression; r
\0.054, P[0.054). In contrast, the
RAW of non-infected females was negatively related to
carapace width (r
=0.325, P\0.0005) as was the case
also for infected females (scarred and with externae) within
the same size range as non-infected females (r
P=0.030). Hence, regardless of infection status, the rel-
ative abdominal width (RAW) increases with size/age in
female crabs, but not in males.
In the Rønbjerg sample, the width of the sixth abdom-
inal segment as a function of carapace width (Fig. 1a–d)
was used to analyse the parasite-induced abdominal
broadening in male crabs. Width of segment 6 increased
linearly with carapace width for non-infected females, non-
infected males and infected males, albeit at a significantly
higher rate in females than in males irrespective of the
infection status of the latter [Fig. 3a; equality of slope
among groups: Standardized Major Axis (SMA) analysis,
T=200.78, P\0.0005; post hoc test: females versus
male groups, P=0.0001]. But whereas the slope of
infected and non-infected males was similar (post hoc test,
P=0.687), suggesting similar metric modification
regardless of size/age, infected males generally attained a
broader abdomen than non-infected (by 12.4 % based on
grand means) (Fig. 3a; equality of grand means: SMA on
square-root transformed data, Wald test, W
P\0.0005). Similar results were obtained also for the
width of the fifth abdominal segment (data not shown),
suggesting that infection results in a broadening of the
entire abdomen. Not only the width but also the length of
Fig. 2 Abdominal and claw dimension of infected and uninfected
Carcinus maenas from Venø Bay, Bjørndrup and Lovns Broad
combined. aBox-plot (mean, SE, range) of relative abdominal width
(RAW) of infected females with externae or scar (FI,n=49), non-
infected females (FN,n=90), infected males with externae (ME,
n=71), infected males with scars (MS,n=45) and non-infected
males (MN,n=49). Median RAW differs significantly among
infection status categories (Kruskal–Wallis test, v
P\0.0005). Lines above box-plots connect statistically similar
categories according to post hoc test correcting for multiple compar-
isons (Pvalues given). All other pair-wise comparisons demonstrated
significantly different RAW (P\0.0005). bBox-plot (mean, SE,
range) of the claw:carapace ratio (claw height divided by carapace
width). Sample sizes and category abbreviations: see above. Median
claw:carapace ratio differs significantly among categories (Kruskal–
Wallis test, v
=151.239, P\0.0005). Lines above box-plots
connect statistically similar categories according to post hoc test
correcting for multiple comparisons (Pvalues given). All other pair-
wise comparisons demonstrated significantly different claw:carapace
ratios (P\0.022)
2018 Mar Biol (2012) 159:2015–2023
the abdomen of males increases following infection. As is
the case for the width, the length of the sixth abdominal
segment increased linearly with carapace width for all three
analysed groups of crabs, albeit at a significantly higher
rate in females than in the two male groups (Fig. 3b;
equality of slope among groups: SMA, T=113.20,
P=0.0001; post hoc test: females versus male groups,
P=0.0001). Whereas the slope of infected and non-
infected males was similar (post hoc test, P=0.739),
infected males generally attained a longer sixth abdominal
segment than non-infected (by 5.8 % based on grand
means) (Fig. 3b; equality of grand means: SMA, Wald
test, W
=75.34, P\0.0005). Hence, the abdomen of
sacculinized males is generally morphologically feminized,
but, in a male way: infected males do not adopt the inherent
allometric relationship characteristic of females.
Accompanying these abdominal changes of sacculinized
males, the usually fused third to fifth segments (Fig. 1d)
develop an articulation, although they never become
capable of independent movements as in females. In
addition, many of the sacculinized males acquired shorter
or longer setae along the margin of the abdomen as females
also possess (Fig. 1b, c). However, in not a single case did
they develop any trace of the setose pleopods 2–5 char-
acteristic for females. The morphology of these pleopods
also appeared unaffected by infection in females.
Fig. 3 Dimensions of abdomen, copulatory appendages and peropods
(legs) as a function of carapace width (CW) in infected and uninfected
Carcinus maenas from Rønbjerg. aStandardized Major Axis (SMA)
analysis of the width of the sixth abdominal segment for infected
males (open circle;n=84; y=0.173x?0.498; r
P\0.0005), non-infected males (closed circle;n=118;
y=0.169x-0.432; r
=0.922, P\0.0005) and non-infected
females (open square;n=109; y=0.530x-8.687; r
P\0.0005). bStandardized Major Axis (SMA) analysis of the
length of the sixth abdominal segment for infected males (open circle;
n=84; y=0.173x?0.498; r
=0.860, P\0.0005), non-infected
males (closed circle;n=118; y=0.169x-0.432; r
P\0.0005) and non-infected females (open square;n=109;
y=0.530x-8.687; r
=0.673, P\0.0005). c. Standardized Major
Axis (SMA) analysis of the length of the copulatory appendage
(pleopod 1) for infected males (open circle;n=84;
y=0.264x?0.187; r
=0.949, P\0.0005) and non-infected
males (closed circle;n=117; y=0.255x?1.017; r
P\0.0005). d. Standardized Major Axis (SMA) analysis of the
length of the longest third pereopod (second walking leg) for infected
males (open circle,n=77; y=1.47x-6.551; r
P\0.0005), non-infected males (closed circle;n=107;
y=1.49x-5.796; r
=0.949, P\0.0005) and non-infected
females (open square;n=100; y=1.22x?1.16; r
Mar Biol (2012) 159:2015–2023 2019
Male copulatory appendages
In the combined Venø Bay, Bjørndrup and Lovns Broad
samples, the length of the first pair of the copulatory
appendages was positively related to carapace width in all
three male categories: non-infected, scarred and externae
present (Linear regression, r
[0.809, P\0.0005). Cor-
rected for carapace width (i.e., the appendage:carapace
ratio), there was no statistically significant effect of
infection status on the relative size of these appendages
(One-way ANOVA, F
=2.099, P=0.126). An SMA
analysis of the Rønbjerg data demonstrated a small but
significant length reduction in the copulatory appendages
of infected individuals (2.2 % based on grand means)
(Fig. 3c; equality of slope: T=1.115, P=0.296; equality
of grand means: Wald test, W
=21.402, P\0.0005).
However, the morphology of the appendages seemed
Claw dimensions
In the combined Venø Bay, Bjørndrup and Lovns Broad
samples, claw height (Fig. 1g) was positively related to
carapace width in all investigated crab categories (Linear
regression, r
[0.638, P\0.0005). Corrected for cara-
pace width (i.e., claw:carapace ratio), relative claw height
was significantly affected by gender and male infection
status (Fig. 2b). Infected and uninfected females had sim-
ilar sized claws that were significantly smaller than those of
males irrespective of their infection status. Sacculinized
male crabs possessing an externa expressed a significantly
smaller claw:carapace ratio than non-infected males,
thereby approaching the claw dimensions of females. In an
analysis including also the female categories, scarred males
could not be statistically separated from either non-infected
males or males with externae (see Fig. 2b). But a separate
analysis including solely the three male categories suggests
that the relative claw size of scarred males is similar to
those with externae, but significantly smaller than those of
non-infected males (Kruskal–Wallis test, v
P\0.0005. Post hoc test: scarred versus externae,
P=1.000; scarred versus non-infected, P\0.0005).
Hence, infection by Sacculina in males results in a claw
size intermediate between non-infected males and females.
Pereopod length
In the Rønbjerg sample, the length of the longer third
pereopod (Fig. 1h) increased linearly with carapace width
for non-infected females, non-infected males and infected
males, albeit at a significantly lower rate in females than in
males irrespective of infection status of the latter (Fig. 3d;
equality of slope among groups: SMA, T=51.844,
P=0.0001; post hoc test: females versus male groups,
P=0.0001). Whereas the slope of infected and non-infec-
ted males was similar (post hoc test, P=0.604), infected
males generally attained shorter pereopods (8.1 % shorter
based on grand means) than non-infected males (Fig. 3d;
equality of grand means: SMA, Wald test, W
P\0.0005). Thus, as for the abdomen, the walking legs of
sacculinized males are morphologically feminized, but
without adopting the inherent female allometry.
Modification of male crabs
Most male C. maenas parasitized by S. carcini showed a
modification of secondary sexual characters which can be
summarized as follows: a redivision of the abdomen, which
broadens to various degrees albeit rarely to an extent
comparable to that of healthy females (Figs. 2a, 3a); sac-
culinized males acquire marginal setae on the abdomen
(Fig. 1c); the length of the abdomen, as expressed by the
sixth segment (Fig. 3b), shows a slight increase which, in
companion with the increase in width, results in an overall
larger abdomen; a slight diminution of the copulatory
appendages (expressed by pleopod 1, see Fig. 3c); and no
additional pleopods appear. The claws show the highest
degree of modification, since they often tend to approxi-
mate those of normal females of same size (Fig. 2b).
Finally, the walking legs are reduced in length as expressed
by the third pereopods (Fig. 3d), thereby approaching the
relatively shorter female pereopods. These results largely
agree with those of Potts (1909), Foxon (1940) and Werner
(2001), who studied the same association but only con-
sidered the modification in abdominal shape, and also those
of Day (1935), who examined males of L. holsatus para-
sitized by S. carcini. As described by Veillet (1945),
S. carcini causes much more modification of males when
parasitizing C. aestuarii, a sibling species of C. maenas
found in the Mediterranean. These modifications comprise
a resegmentation of the abdomen, which may become
nearly as broad as in sexually mature females, acquisition
of pronounced marginal setae, and appearance of female-
like biramous and setae pleopods (swimmerets) that often
become asymmetrically developed. The copulatory
appendages become shorter and more fragile, and the
second pleopod disengages from the first and may acquire
segmentation and setae. The claws also diminish in size.
Nielsen (1970) similarly observed that the modification of
males caused by hermit crab infesting rhizocephalans may
vary with host species.
Even more extensive modification of sacculinized males
occur in other species of crabs parasitized by sacculinid
2020 Mar Biol (2012) 159:2015–2023
rhizocephalans. Infested males not only may acquire an
abdomen as broad and vaulted as in the female counterpart,
but may also show a varying number of pleopods, degen-
eration or disappearance of the copulatory appendages, and
reduction in the size of the chelae (Giard 1886; Smith
1910; Okada and Miyashita 1935; Matsumoto 1952;
George 1959; Galil and Lu
¨tzen 1995). The almost total
feminization of Portunus sanguinolentus (Herbst, 1783) by
Heterosaccus ruginosus Boschma, 1931, led Nair and
Gurumani (1956) and Srinivasagam (1982) to believe that
each of the 179 sacculinized crabs investigated were of the
female sex. This highlights the importance of taking par-
asitic feminization into account in population studies of
sacculinized crab populations.
Several studies have shown that the degree to which
male hosts become modified decreases with size (Pe
1933; Day 1935; Veillet 1945). The explanation given for
this is that the modifications occur stepwise and at each
moult and that smaller crabs on an average go through
more moults than larger ones before the cessation of
moulting caused by the parasite sets in. Our data support
this explanation because our analyses of covariance dis-
close that smaller sacculinized male crabs are relatively
more modified than larger males (Fig. 3). This agrees with
the observations made by Foxon (1940), but is contrary to
those of Potts (1909), two authors who studied the same
parasite-host association as we did. These covariance
analyses also suggest that the amount of modification in
exact metric terms to be similar in infected males regard-
less of their size.
Modification of female crabs
Parasitized females of C. maenas did not exhibit any
morphological modification. The mean relative abdominal
width and the claw size remain unchanged (Fig. 2). This is
concordant with most other studies showing that sacculi-
nized females undergo little, if any, modifications (Day
1935; Hartnoll 1967; Phillips and Cannon 1978; Yamag-
uchi and Aratake 1997; Werner 2001). Nevertheless, some
crabs, including C. aestuarii parasitized by S. carcini, may
be subject to major changes (Veillet 1945). Although such
cases are deceptively known as hyperfeminization, the
abdomen is usually of normal width and only rarely
excessively broadened as seen, for instance, in Callinectes
sapidus Rathbun, 1896, parasitized by Loxothylacus tex-
anus Boschma, 1933 (Reinhard 1950). Moreover, rather
than increasing in size, the pleopods may degenerate more
or less completely (Okada and Miyashita 1935; Matsumoto
1952; Galil and Lu
¨tzen 1995). In female crabs of some
species, the adult secondary sexual characters may appear
at a considerable smaller body size than usual as a result of
sacculinization (Smith 1906,1910;Pe
´rez 1933; Veillet
1945; Vernet-Cornubert 1958). In the very few cases where
the relative claw size in sacculinized females has been
analysed, it never differs from that of non-parasitized
females (Veillet 1945; Yanagimachi and Aratake 1997).
Survival of externae on modified crabs
Veillet (1945) and Lu
¨tzen (1984) showed that the ratio of
externally infected female crabs to that of the males
gradually increases with the age of the externae. In our
presently unpublished material, comprising more than
17,000 parasitized C. maenas from Limfjorden, the pro-
portion of infected male crabs with scars from lost externas
is 23.8 %, while the same proportion for female crabs is
only 14.6 %. Together, this suggests that females are better
hosts. The much broader abdomen of the female, particu-
larly in the larger individuals having relatively broader
abdomen, offers a better protection of the externa than the
narrower abdomen of males. Regeneration of a lost externa
occurs only rarely in S. carcini (Lu
¨tzen 1981). Externa loss
usually leads to the death of the parasite. This means that
the survival rate of the parasite is favoured by the devel-
opment of a broad female-like abdomen that protects
against accidental and loss of the externa. In the sacculinid
Heterosaccus dollfusi Boschma, 1960, the parasite induces
an abdomen as broad as that of healthy females of its host
Charybdis longicollis Leene, 1938. This results in an
equally high survival of the externae in both host sexes
(Galil and Lu
¨tzen 1995). This is born out by the fact that
the number of scarred crabs, each indicating a lost externa,
makes out only 2.3 % of the number of crabs with exter-
nae, a percentage that is much lower than in most other
species of sacculinized crabs (Veillet 1945;Lu
¨tzen 1984).
This probably means that most externae of H. dollfusi stay
with the host for life and are rarely lost. In Portunus
pelagicus L., 1758, sacculinized males develop an abdo-
men almost as broad as that of the females, and the per-
centage of scarred males is accordingly also low, \1%
(Weng 1987). Our data on S. carcini infesting C. maenas
show a more variable pattern. In contrast to the examples
mentioned above, the degree to which S. carcini modifies
the abdomen of a male host varies greatly from one host
specimen to another; from almost no change to close to
female proportions (Figs. 1,2,3). The data furthermore
demonstrate that crabs with scars from lost externae show
significantly less pronounced feminization of the abdomen
than found in males, still carrying viable externae (Fig. 2a).
This may reflect the presence of a co-evolutionary arms
race scenario between host and parasite: a parasite unable
to cause a male host to produce a protectively broadened
female-like abdomen is selected against. The host, on the
other hand, is exposed to strong selection pressure to pre-
vent the parasite-induced broadening of the abdomen. The
Mar Biol (2012) 159:2015–2023 2021
less morphological affected an infected male host, the
greater is the chance that the emerging externa is physi-
cally damaged and dies due to the poor protection provided
by a narrow male abdomen. The death of the parasite might
enable the crab to resume moulting and eventually repro-
duce. In contrast to the sacculinids on C. longicollis and
P. pelagicus, where this arms race seems already won by
the parasite, the S. carcini/C. maenas system may be at a
transitional evolutionary state, where full feminization of
the abdomen in male hosts has been only partly estab-
lished. As a result, the capability of each individual parasite
to modify the host still varies greatly within the population.
This calls for experimental studies on the extent to which
C. maenas that loose a S. carcini externa resume growth
and reproduction. Although scarred C. maenas have a
higher mortality rate than uninfected crabs, they may sur-
vive for an extended period of time (Lu
¨tzen 1981). The
additional parasitically induced morphological effects on
the male (reduced copulatory appendages, chelae and
pereopods) cannot easily be interpreted as advantageous to
parasite survival. They may simply be pleiotropic side
effects from the main adaptive value of broadening the
abdomen through hormonal manipulation. However, pos-
sibly also less understood physiological or behavioural
advantages of feminizing male hosts could be involved.
Phylogenetic remarks
Species of the family Sacculinidae Lilljeborg, 1860, exhibit
a number of surprisingly uniform morphological traits.
Attached to the underside of the brachyuran host’s abdo-
men, the left and right sides of the externa are flattened to
fit into the narrow space between the sternum and the
abdomen, with the dorsal sides and ventral sides always
directed towards the same sides with respect to the host’s
abdomen. Molecular data have nevertheless shown the
family and the type genus Sacculina Thompson, 1836, to
be diphyletic (Glenner and Hebsgaard 2006). To date, few
species of Sacculina have been relegated to the Sacculin-
idae s. str., which besides the type species, S. carcini,
probably contains all species of Heterosaccus Smith 1906
and Loxothylacus Boschma, 1928. No family name has yet
been proposed for the other group, which is known with
certainty to contain only a few species that were earlier
referred to as Sacculina plus all three species of Polyascus
Glenner, Lu
¨tzen and Takahashi, 2003.
When comparing morphological modifications caused
by sacculinid and non-sacculinid species of the ‘‘Saccu-
linidae’’, the general pattern is the same: males invariable
acquire a broadened and resegmentated abdomen, which
may or may not develop pleopods, and the copulatory
appendages may degenerate while the claws almost always
become reduced in size. The females, in contrast, are rarely
affected. The underlying physiological cause of the femi-
nization of parasitized males is still unknown. It has been
explained as a parasitic destruction of the androgenic
gland, which in healthy crabs induces masculinisation in
the males (Veillet and Graf 1958; Høeg 1995), but alter-
native physiological pathways might be possible. In any
case, it is most likely that the mechanism operating in both
groups of ‘sacculinids’ is identical.
Acknowledgments We are very grateful to the Carlsberg Founda-
tion for covering all expenses connected with the study (grant no.
2008-01-0491). We also wish to thank the staff of the Danish
Shellfish Center, Nykøbing Mors, Denmark, for collecting some of
the material and providing laboratory facilities, and Dr. David R.
Nash, Section for Social Evolution, Department of Biology, Univer-
sity of Copenhagen, Denmark, for advice and assistance.
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... In infected male crabs, spermatogenesis stops and the testes degenerate. These castrated males progressively differentiate feminized morphology; they acquire a broader and longer abdomen where the parasite's externa will develop in place of crab eggs (Kristensen et al. 2012). In parallel, infected males begin to exhibit behaviors of brooding typically exhibited by non-parasitized females (migrating where brooding females are present, and grooming the externa; Sloan 1984 and references therein). ...
... Here, castration evolved as an adaptation to exploit female hosts, the most abundant "resource" available for the parasite (D. magna are mostly parthenogenetic). Observations of behavioral and morphological changes induced by rhizocephalan parasites all suggest advantages for the parasite, but not for the decapod host (Sloan 1984, Kristensen et al. 2012. The development of a broader abdomen allows the parasite's externa to have more space, and grooming behavior allows the externa to be oxygenated. ...
This chapter reviews the influences of environmental factors on sex determination, sex ratios, and reproductive behavior in the Crustacea, focusing in particular on amphipod and isopod examples. A range of abiotic and biotic environmental factors influence reproduction in Crustacea, including temperature, day length, pollutants, and parasites. Individual crustaceans may benefit from these environmental influences, but in other cases, reproductive biology responses to biotic and abiotic environments may be detrimental to individual fitness. Environmental Sex Determination (ESD) falls into the former category. ESD is an adaptive mechanism of sex determination that is rare, but has evolved in diverse taxa. Evidence from gammarid amphipods is used to explore the evolution of ESD in response to a patchy environment. While ESD is an adaptive mechanism of sex determination, the impact of other environmental factors can be very costly. Parasitic castrators can lead to a reduction or total cessation of reproduction in crustacean hosts, driving population declines. In contrast, parasitic feminizers convert male hosts into females, enhancing maternal parasite transmission but also leading to sex ratio distortion in the host population. The chapter discusses parasite-host coevolutionary conflict and reviews evidence that selection on the host in response to parasitic sex ratio distortion has led to altered mate choice in amphipods, and to the evolution of a novel system of sex determination in isopods. Human-induced environmental influences can also be seen in Crustacea, and the chapter discusses how parasites, ESD, and endocrine-disrupting chemicals can each affect sex determination and lead to abnormal intersex phenotypes. It ends by highlighting areas for future research on the diverse world of crustacean reproduction.
... As a result of infection, the host becomes castrated, reducing individual host fitness to zero (Alvarez et al. 1995;Reisser and Forward 1991;Walker et al. 1992;Galil 2007, 2011). Infected crabs protect and groom the parasite externae: these maternal behaviors are also exhibited by male crabs, commonly referred to as "male feminization" Galil 2007, 2011;Kristensen et al. 2012). Rhizocephalan infection can also change host morphology: parasitized crabs (particularly males) have wider abdomens than those that are uninfected (Kristensen et al. 2012). ...
... Infected crabs protect and groom the parasite externae: these maternal behaviors are also exhibited by male crabs, commonly referred to as "male feminization" Galil 2007, 2011;Kristensen et al. 2012). Rhizocephalan infection can also change host morphology: parasitized crabs (particularly males) have wider abdomens than those that are uninfected (Kristensen et al. 2012). Altogether, these highly impactful physiological (castration, nutrient extraction, morphological changes) and behavioral (protection, male feminization, foraging changes) effects of rhizocephalan infection are strong indicators of the potential for population and community level influences, particularly in systems where the host has little prior experience with the parasite, or has escaped its parasite for a period of time (Alvarez et al. 1995;Innocenti and Galil 2007;Mouritsen et al. 2018). ...
Parasites can greatly affect the behavior of their hosts, influencing how they respond to biotic and abiotic factors within their communities. Some parasites are particularly impactful, causing significant reproductive and behavioral changes in hosts relative to uninfected conspecifics. In eastern North America, a non-native parasitic barnacle, Loxothylacus panopaei (Gissler, 1884), has severe reproductive impacts on native panopeid mud crab hosts, resulting in castration. Moreover, the parasite has been documented to induce significant behavioral changes, such as reducing mud crab activity, influencing predator-prey relationships, and enhancing hiding behaviors in infected host crabs. Yet much remains to be understood regarding the host's ability to escape predators in heterogeneous environments. We investigated the effects of L.panopaei parasitism on mud crab (flatback mud crab, Eurypanopeus depressus (Smith, 1869)) survival in simple versus complex habitats. In lab mesocosm experiments, habitat heterogeneity was manipulated using oysters and gravel, and predatory pressures came from two common predatory crabs in southeast Atlantic estuaries: the Atlantic mud crab, Panopeus herbstii (H. Milne Edwards 1884) and the stone crab, Menippe mercenaria (Say, 1818). We found L.panopaei-infected E. depressus crabs to have the lowest survival rates in the simple gravel habitat, while the crabs with the highest survival were uninfected crabs in the complex oyster habitat. Moreover, we detected differences between uninfected and infected crabs in habitat usage (oyster versus gravel) within the complex habitat. This study demonstrates the complexity of predator-prey dynamics in the face of impactful parasitism and global change, including the introductions of species to new communities where they may have strong impacts on host populations and community interactions.
... Infected hosts are often more docile (Bishop and Cannon 1979;Shields and Wood 1993;Horacio et al. 2020). Feminisation results from direct damage to the androgenic gland, the sex determining organ in crustaceans (Zerbib et al. 1975;Rubiliani and Payen 1979), which, when damaged prior to maturation, leads to modifications of the secondary sexual characters during moulting (Kristensen et al., 2012). Castration arises from interruption of reproductive hormones or through the metabolic cost of infection (Andrieux 1974;Rubiliani 1983). ...
This chapter represents the first qualitative review of the protistan and metazoan parasites of Crustacea.
... A higher rhizocephalan prevalence in female compared to male crab hosts has also been observed in other rhizocephalan species, sometimes also with even more (Rasmussen 1973;Høeg and Lützen 1995;Mouritsen et al. 2018). It has been suggested that this difference in prevalence does not result from a preferred settlement of infective stages on female crabs but rather stems from a higher survival of parasites in females as their broader abdomen gives better protection for the parasite and its externa (Sloan 1984(Sloan , 1985Reisser and Forward 1991;Høeg and Lützen 1995;Kristensen et al. 2012). However, further studies are necessary to investigate whether this is also the case in P. leptodiae. ...
Rhizocephalan cirripedes are a very unique group of parasites infecting decapod crustaceans, but apart from a few well-studied species, little is known on their ecology and impact on hosts. Here we report on the results of a 14-month study of infestations of the rhizocephalan Parasacculina leptodiae in the rocky shore crab Leptodius exaratus along the shores of Kuwait in the Persian Gulf (Arabian Gulf). Monthly samples along an intertidal gradient revealed a slightly higher prevalence of P. leptodiae in female (18%) compared to male crabs (11%) and marked differences in prevalence among the sampling sites. Crabs from more sheltered locations in Kuwait Bay showed lower prevalence of P. leptodiae compared to crabs from more exposed sites. Seasonal patterns were largely absent, but prevalence in female crabs showed some monthly variation depending on the site. Rhizocephalan prevalence was generally highest in both crab sexes at the lower shores. This possibly resulted from lower exposure of crabs to infective stages in the higher intertidal and movements of infected crabs to lower parts of the shore. Prevalence of ovigerous females significantly declined with increasing local parasite prevalence. This suggests that the well-known castrating effects of rhizocephalans on individual hosts can also affect local crab reproduction at the population level which has not been shown before. Our results indicate that the rhizocephalan P. leptodiae is a common parasite of the rocky shore crab L. exaratus along the shores of Kuwait, with potential effects on the crab's population dynamics which warrants further study.
... For reproduction, the female host is forced to bear the parasitic barnacle eggs instead of its own, while in the male host, spermatogenesis is arrested and the gonadal tissue is degenerated, but does not disappear entirely [27]. Furthermore, changes in behavioral and external morphology, such as widening of the abdomen in parasitized males, cause the male host crabs to take on a feminine appearance [28]. For adult female barnacles, the body is made up of internal and external parts. ...
Full-text available
The Chinese mitten crab (Eriocheir sinensis) is a representative catadromous invertebrate of the Yangtze River and a commercial species widely cultivated in China. Both cultivated and wild crabs suffer from a variety of parasites and pathogens, which can result in catastrophic economic losses in aquaculture revenue. Polyascus gregaria, a parasitic barnacle with a highly derived morphology, is specialized in invading these crabs. This study examines the immunological mechanism in E. sinensis infected with P. gregaria. Tandem mass tags (TMT), a specialized method of mass-spectrometry, was used to analyze the infection by P. gregaria resistance at the protein level. In the hepatopancreas of infected crabs, 598 proteins differentially expressed relating to physiological change, of which, 352 were upregulated and 246 were downregulated. Based on this differential protein expression, 104 GO terms and 13 KEGG pathways were significantly enriched. Differentially expressed proteins, such as ATG, cathepsin, serpin, iron-related protein, Rab family, integrin, and lectin, are associated with the lysosome GO term and the autophagy-animal KEGG pathways, both of which likely relate to the immune response to the parasitic P. gregaria infection. These results show the benefit of taking a detailed, protein-level approach to understanding the innate immune response of aquatic invertebrates to macroparasite infection.
... Female D. patagonicus masculinization was only apparent by the absence of setae on the inner branch of the pleopods. Taking into consideration the development of biramous pleopods, the high proportion of males without gonopods and the widening of the abdomen, it can be stated that male D. patagonicus suffer a high degree of feminization (Yamaguchi & Aratake 1997), in contrast to the pattern observed in other rhizocephalan parasite−host systems, such as S. carcini infecting C. maenas, where morphological feminization is less apparent (Kristensen et al. 2012). Although gonad castration of both sexes of D. patagonicus was the general pattern observed in our study, the finding of 1 infected male displaying mature gonads and spermatophores in the vas deferens suggests that this may not be absolute in some specimens as reported for the host−parasite association between P. pelagicus and S. granifera (Shields & Wood 1993). ...
The system formed by a still-unidentified rhizocephalan infecting the Patagonian stone crab Danielethus ( Platyxanthus ) patagonicus (A. Milne-Edwards, 1879) was analyzed in northern Patagonia. Out of 3222 crabs sampled, mean prevalence of externae was 2.1%, while corrected mean prevalence based on observations of externae, scars or other indicators of infection was slightly higher (3.01%; N = 2100). Prevalence was higher in males (4.47%) than in females (1.44%). Parasitized males were morphologically feminized, while females showed no hyper-feminization. Although most parasitized crabs showed only 1 externa, 2 externae were observed in some individuals. The parasite externae were only present in intermediate-sized crabs (26.6-99.7 cm carapace width). While scanning electron microscopy images allowed detection of the ‘smooth-surface-balloon’ type of retinacula on the inner surface of the externae, typical of the Sacculinidae and Peltogastridae, the position of the mantle opening relative to the stalk, the receptacle location and the shape of the externae suggest that the parasite belongs to either the genus Sacculina or to the recently erected Parasacculina (Polyascidae).
... Sacculina carcini has no mouth, gut, respiratory organs, excretory organs or an alimentary canal during its parasitic life cycle stage (Bresciani and Høeg 2001). The effects of an infection by S. carcini on C. maenas include: parasitic castration, behavioural feminization of males, tissue changes, growth limitation or even a complete stop of the moult cycle (Powell and Rowley 2008, Kristensen et al. 2012, Waser et al. 2016. The reproductive organ of S. carcini, the so-called externa, develops outside of its host and is the only body part visible to the naked eye. ...
Full-text available
Traditional bulk isotopic analysis is a pivotal tool for mapping consumer–resource interactions in food webs but has largely failed to adequately describe parasite–host relationships. Thus, parasite–host interactions remain undescribed in food web frameworks despite these relationships increasing linkage density, connectance and ecosystem biomass. Compound‐specific stable isotopes from amino acids provides a promising novel approach that may aid in mapping parasite–host relationships in food webs. Here we apply a combination of traditional bulk stable isotope analyses and compound‐specific isotopic analysis of nitrogen in amino acids to examine resource use and trophic interactions of five parasites from three hosts from a marine coastal food web (Wadden Sea, European Atlantic). By comparing isotopic compositions of bulk and amino acid nitrogen, we aimed to characterize isotopic fractionation occurring between parasites and their hosts and to clarify parasite trophic positions. Our results indicate that parasitic trophic interactions were more accurately identified using compound‐specific stable isotope analysis due to removal of underlying source isotopic variation for both parasites and hosts. The compound‐specific method provided clearer trophic discrimination factors in comparison to bulk isotope methods. Amino acid compound specific isotope analysis has widely been applied to examine trophic position within food webs, but our analyses suggest that the method is particularly useful for clarifying the feeding strategies for parasitic species. Baseline isotopic information provided by source amino acids allows clear identification of the fractionation from parasite metabolism by integrating underlying isotopic variations from the host tissues. However, like for bulk isotope analysis, the application of a universal trophic discrimination factor to parasite–host relationships remains inappropriate for compound‐specific stable isotope analysis. Despite this limitation, compound‐specific stable isotope analysis is and will continue to be a valuable tool to increase our understanding of parasitic interactions in marine food webs.
... Another hallmark of host manipulation by rhizocephalans is the feminization of male hosts, which includes changes in behaviour (Brockerhoff et al., 2010;Høeg, 1995;Kristensen et al., 2012). We found that males exhibited a greater transcriptional response to infection compared to females, which may reflect differences in how L. panopaei manipulates its host depending on its sex. ...
By shuffling biogeographic distributions, biological invasions can both disrupt long‐standing associations between hosts and parasites and establish new ones. This creates natural experiments with which to study the ecology and evolution of host‐parasite interactions. In estuaries of the Gulf of Mexico, the white‐fingered mud crab (Rhithropanopeus harrisii) is infected by a native parasitic barnacle Loxothylacus panopaei (Rhizocephala), which manipulates host physiology and behavior. In the 1960s, L. panopaei was introduced to the Chesapeake Bay and has since expanded along the southeastern Atlantic coast, while host populations in the northeast have so far been spared. We use this system to test the host’s transcriptomic response to parasitic infection and investigate how this response varies with the parasite’s invasion history, comparing populations representing (1) long‐term sympatry between host and parasite, (2) new associations where the parasite has invaded during the last sixty years, and (3) naïve hosts without prior exposure. A comparison of parasitized and control crabs revealed a core response, with widespread downregulation of transcripts involved in immunity and molting. The transcriptional response differed between hosts from the parasite’s native range and where it is absent, consistent with previous observations of increased susceptibility in populations lacking exposure to the parasite. Crabs from the parasite’s introduced range, where prevalence is highest, displayed the most dissimilar response, possibly reflecting immune priming. These results provide molecular evidence for parasitic manipulation of host phenotype and the role of gene regulation in mediating host‐parasite interactions.
Polyascus gregaria is a specialized crustacean parasite of Chinese mitten crab; however, only limited information on interactions between parasite and its host is available. This study examined interactions between P. gregaria and Chinese mitten crab with regard to immune‐related enzyme activities and expression of respective genes in the hepatopancreas. To further elucidate the pathogen–host interactions, untargeted gas chromatography–mass spectrometry (GC–MS) metabolomics was used to analyse changes in metabolites in response to P. gregaria infection. Superoxide dismutase, acid phosphatase and alkaline phosphatase activities were significantly increased in parasitized crabs, whereas phenoloxidase activity was significantly decreased. Moreover, the expression of three immune‐related genes, that is proPO, Toll1 and Toll2, was markedly downregulated in parasitized crabs. In the metabolomic assay, 73 differential metabolites were identified, and they were significantly enriched in 71 pathways. Among these metabolites, 58 were significantly upregulated and 15 were downregulated. Lysolipids lysoPE, lysoPC, lysoPG, LysoPI and lysoPS were the most strongly upregulated metabolites, and 9‐cis‐retinol, glycerophosphocholine and 5‐thymidylic acid were the top three downregulated metabolites. Most of these metabolites were enriched in the glycerophospholipid metabolism pathway, which was one of the most significantly activated pathway responses to P. gregaria infection. This increase in lysoglycerophospholipids caused major structural and functional abnormalities in the membranes of host tissues, especially in the hepatopancreas. We propose that long‐term infection with P. gregaria induces silence of the innate immune system, disturbs intracellular homeostasis and causes cell membrane immune‐related dysfunction in Chinese mitten crab. These results may help us better understand P. gregaria infection in Chinese mitten crab.
The morphological modifications caused by Sacculina polygenea in the grapsid crab Hemigrapsus sanguineus were examined. Parasitized males carrying externa were divided into seven stages of feminization by the degree of reduction of the first and second pleopods and the appearance of biramous pleopods on the third to fifth abdominal segments. All males examined retained first pleopods and most of them were Stage I or II. The development of femaletype biramous pleopods rarely occurs. Only 10.1% crabs were in advanced stages of feminization. Enlargement of the abdomen and reduction of chela height in parasitized males were pro nounced in small males and less so in larger males. Modification caused by the rhizocephalan parasite likely proceeds from when the host is young and small.
A study of major events in the life cycle of Sacculina carcini parasitizing shore crabs, Carcinus maenas (L.), was undertaken at a northern boreal locality (c. 56° N). During 1979 –82, 28 388 crabs were collected fairly regularly from May to September, supplemented with smaller samples from October to April. Infestation ranged between 1.85 and 2.90 %, female crabs being less often infected than males. The internal phase of the life cycle is calculated to last at least 33 –34 months. Observations in the field and on 200 sacculinized crabs kept under surveillance in cages in the sea showed that the externae normally break through the host’s abdomen in June –July. Growth of the externae does not occur until c. 1 July and only if cells from pelagic male cyprids are transferred to the externa’s receptacles. At 15 –18° C the externae grow to maturity and a width of 14 –17.5 mm in 17 –24 days. The main breading season extends from mid –July to September/October during which up to 6 batches each containing 1 –3 × 105 eggs are produced at a minimum interval of 12 days. The production of Sacculina larvae peaks in August –September when the 0-group of crabs is most abundant. From November to April breeding stops almost completely but the externae which survive the winter enter a second, shorter breeding period in May or June in which male cyprids, indispensible for the growth of the small externae, are produced. Most externae die and drop off the host before they are a year old; old ones survive better on female than on male crabs.
ABSTRACT Since 1993, Heterosaccus dollfusi has been a very common parasite on the crab Charybdis longicollis along the Mediterranean coast of Israel. It accompanied from the Red Sea this Lessepsian migrant crab. The parasite is more common on male than female crabs, where it becomes external on hosts of many sizes shortly after a molt and undergoes characteristic growth stages. The parasite usually causes the complete loss of pleopods in both sexes and a feminine broadening of the abdomen in male crabs. Parasite survival is the same in both sexes of the host. More than one parasite per host is frequent, each probably originating from an individual cypris larva rather than from asexual budding. Hosts with single parasites outlive those with multiple infections.