847
Acanthocephalan size and sex affect the modification of
intermediate host colouration
D. P. BENESH 1*, O. SEPPÄLÄ 2 and E. T. VALTONEN 3
1
Department of Evolutionary Ecology, Max-Planck-Institute for Evolutionary Biology, August-Thienemann-Strasse 2,
24306 Plön, Germany
2
EAWAG, Department of Aquatic Ecology, and ETH-Zürich, Institute of Integrative Biology, Überlandstrasse 133,
8600 Dübendorf, Switzerland
3
Department of Biological and Environmental Science, POB 35, FI-40014 University of Jyväskylä, Finland
(Received 5 January 2009; revised 10 February, 10 March and 16 March 2009; accepted 16 March 2009; first published online 19 May 2009)
SUMMARY
For trophically transmitted parasites, transitional larval size is often related to fitness. Larger parasites may have higher
establishment success and/or adult fecundity, but prolonged growth in the intermediate host increases the risk of failed
transmission via natural host mortality. We investigated the relationship between the larval size of an acanthocephalan
(Acanthocephalus lucii) and a trait presumably related to transmission, i.e. altered colouration in the isopod intermediate
host. In natural collections, big isopods harboured larger worms and had more modified (darker) abdominal colouration
than small hosts. Small isopods infected with a male parasite tended to have darker abdominal pigmentation than those
infected with a female, but this difference was absent in larger hosts. Female size increases rapidly with host size, so females
may have more to gain than males by remaining in and growing mutually with small hosts. In experimental infections, a
large total parasite volume was associated with darker host respiratory operculae, especially when it was distributed among
fewer worms. Our results suggest that host pigment alteration increases with parasite size, albeit differently for male and
female worms. This may be an adaptive strategy if, as parasites grow, the potential for additional growth decreases and the
likelihood of host mortality increases.
Key words: Acanthocephala, Asellus aquaticus, cystacanth, host exploitation, host phenotype manipulation, intermediate
host, larval life history, sexual dimorphism, trophic transmission.
INTRODUCTION
For trophically transmitted parasites, infectivity to
the next host in the life cycle is only achieved at a certain developmental stage. Consequently, any parasite
traits related to transmission, such as manipulation of
host phenotype (reviewed by Moore, 2002 ; Thomas
et al. 2005), should be expressed only after some
degree of infectivity is achieved (e.g. Bethel and
Holmes, 1974 ; Poulin et al. 1992 ; Pulkkinen et al.
2000 ; Seppälä et al. 2005 ; Franceshi et al. 2008).
However, developing to an infective stage does not
necessarily indicate that the probability of parasite
establishment in the next host is at a fixed level. Invasion success typically varies among infective-stage
individuals with larger parasites often faring better
(Rosen and Dick, 1983 ; Steinauer and Nickol, 2003).
Large larval parasites may also have other fitness
advantages, such as a shorter developmental time to
maturity or higher adult fecundity (Parker et al.
* Corresponding author : Department of Evolutionary
Ecology, Max-Planck-Institute for Evolutionary Biology,
August-Thienemann-Strasse 2, 24306 Plön, Germany.
Tel: +494522763258 ; fax : +494522763310. E-mail :
benesh@evolbio.mpg.de
2003 ; Fredensborg and Poulin, 2005). Prolonged
larval growth, however, has associated costs, such as
an increasing likelihood of natural host mortality and
thus failed transmission. This trade-off between
transitional size and age is the basis for many models
on life-cycle evolution (Rowe and Ludwig, 1991 ;
Stearns, 1992 ; Berrigan and Koella, 1994 ; Abrams
et al. 1996 ; Day and Rowe, 2002 ; Iwasa and Wada,
2006). If a large larval size is very advantageous, then
continued growth may be worth the risk, perhaps
even after parasites have reached an infective stage.
Under these conditions, delayed host manipulation
may be a favourable strategy.
In this study, we investigated the relationship
between the larval size of an acanthocephalan
(Acanthocephalus lucii) and the alteration of intermediate host colouration. Freshwater fishes are the
definitive hosts of A. lucii, usually European perch
(Perca fluviatilis). Parasites mate in the fish’s
intestine and eggs are released into the environment
with the host’s faeces. Intermediate hosts, freshwater
isopods of the species Asellus aquaticus, become infected by ingesting eggs. Parasites develop in the
body cavity of isopods for several weeks before they
reach the infective cystacanth stage (Andryuk, 1979).
Post-infectivity larval size can vary considerably in
Parasitology (2009), 136, 847–854. f Cambridge University Press 2009
doi:10.1017/S0031182009006180 Printed in the United Kingdom
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D. P. Benesh, O. Seppälä and E. T. Valtonen
Table 1. Naturally collected isopods used in the analysis
(The isopods were collected in different seasons and exposed to different treatments in the laboratory.)
Block
Collection
date
N (infected)
Experimental treatment
Reference*
1
2
3
4
5
6
7
Sept. 2005
Sept. 2005
Oct. 2005
May 2006
Aug. 2006
Oct. 2006
Aug. 2006
148 (58)
84 (42)
69 (27)
40 (16)
55 (29)
68 (31)
52 (26)
1
1
1
2
2
2
2
8
Aug. 2006
55 (28)
9
Aug. 2006
47 (21)
Approximately 1 week at 17 xC, 18 h light
Less than 1 week at 17 xC, 18 h light
Eight weeks observation at 17 xC, 18 h light
Two weeks observation at 17 xC, 18 h light
Two weeks observation at 17 xC, 18 h light
Two weeks observation at 17 xC, 18 h light
Four weeks acclimation to 17 xC, 18 h light,
then 2 weeks observation under same conditions
Four weeks acclimation to 11 xC, 12 h light,
then 2 weeks observation under same conditions
Four weeks acclimation to 5 xC, no light,
then 2 weeks observation at 17 xC, 18 h light
2
2
* 1, Benesh et al. (2008) ; 2, Benesh et al. (2009).
A. lucii ; among female cystacanths there can be more
than a 2-fold difference between the smallest and
largest individuals (Benesh and Valtonen, 2007 c).
Much of this variation is explained by isopod size ;
larger hosts harbour larger worms (Benesh and
Valtonen, 2007 b, c). Therefore, parasites in small
isopods may have a lot to gain by remaining in the
host and continuing to grow mutually with it (Benesh
and Valtonen, 2007a, b). The potential payoffs of
remaining in isopods likely differ between parasite
sexes, though. Female cystacanths are larger than
males and their size increases faster as a function
of isopod size, indicating that females allocate more
of the available resources to growth (Benesh and
Valtonen, 2007 c). This suggests that a large transitional size is more important for females than
males, possibly because fecundity increases with
female size, whereas male reproductive success may
only increase with body size under specific forms
of competition (Stearns, 1992). Thus, delaying the
expression of transmission-relevant traits until a
larger size is reached may be particularly profitable
for female worms.
As A. lucii reaches the cystacanth stage, the respiratory operculae of their hosts become darkly pigmented (Brattey, 1983), and this renders the overall
abdominal pigmentation of infected isopods darker
than that of uninfected isopods (Benesh et al. 2008).
Conspicuous isopods are likely to be eaten by fish
(Hargeby et al. 2004, 2005), so the modified colouration of infected isopods presumably increases their
predation risk (Brattey, 1983 ; Seppälä et al. 2008).
Although altered host colouration appears related
to parasite transmission, a direct link has not been
established. This caveat deserves mention because a
recent study found no relationship between intermediate host appearance and predation risk in a different acanthocephalan (Kaldonski et al. 2009). Here
we test (1) if there is a relationship between parasite
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size and host colouration and (2) whether this pattern
differs between male and female parasites. The main
analysis was conducted with naturally infected
isopods. However, natural infections can be problematic, as infection is not a randomly assigned
treatment. Thus, the relationship between colouration and parasite size was also investigated in a
group of experimentally infected isopods.
MATERIALS AND METHODS
Naturally infected isopods
Isopods were collected in 2005 and 2006 from Lake
Jyväsjärvi, Central Finland (62x14kN 25x44kE) for
use in various other experiments (Table 1). At the
end of all experiments, live isopods were frozen in
lake water at x20 xC. At a later date, isopods were
thawed and individually photographed with a Nikon
Coolpix 4500 digital camera (light conditions and
camera settings were described by Benesh et al.
(2008)). After photographs were taken, isopods were
measured to the nearest 0.5 mm and then dissected
to determine infection status (presence/absence of
A. lucii ; number and sex of cystacanths). Worms
reach an advanced state of development in isopods,
so their sex can be easily established based on whether
there are testes or ovarian balls in the body cavity.
Cystacanths were placed in refrigerated tap water
to relax and extend. The length and width of all
cystacanths were measured to the nearest 0.01 mm
using an ocular micrometer on a light microscope.
Worms were considered cylindrical in shape, so
cystacanth volume (mm3) was calculated with the
equation (plw2)/4 where l is worm length and w is
worm width. Additionally, a subsample of worms
(n=116) were dried at 60 xC for 3–4 h and then
weighed to the nearest mg on a microbalance
(Sartorius, SE MA 2.1 g).
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Larval size and host colouration
Host size – parasite size relationship
Using a subset of the isopods listed in Table 1,
Benesh and Valtonen (2007 c) showed that, in singlecystacanth infections, the slope of the correlation
between cystacanth size and isopod size was higher
for female worms than for males. Because this growth
pattern is a major assumption for our hypothesis
of sexually-divergent manipulation strategies, the
relationship between host size and parasite size was
checked using all the collected isopods that harboured a single cystacanth. An analysis of covariance
(ANCOVA) was performed with parasite volume as
dependent variable, worm sex as a fixed factor, and
isopod size as a covariate. A second ANCOVA using
parasite dry mass instead of volume was also performed. Mass and volume measurements need not
give identical results, e.g. if sexual organs (testes vs
ovarian balls) have different weights.
Analysis of isopod colouration
Photographs of whole isopods were analysed using
Adobe Photoshop 7.0 software (Adobe Systems Inc.,
San Jose, CA, USA). The analysis of whole-isopod
photographs was described previously (Benesh et al.
2008). Briefly, all pictures were converted to greyscale and reflectance values for the first, fourth, and
seventh segments were averaged to give a mean value
for body pigmentation. A reflectance value for the
abdomen was also calculated. The scale of reflectance
in the software ranged between 0 (black, 100 % saturation) and 255 (white, 100 % reflectance). Histograms of reflectance of individual pixels within the
analysed areas resembled a normal distribution, so
the mean value of reflectance from each area was
taken as a measure of colouration. Reflectance values
ranged from 41.2 to 126.2 for body colouration
and 32.5 to 142.3 for abdominal colouration. This
method was highly repeatable (Benesh et al. 2008).
Isopods were either uninfected (n=340), infected
with a single male cystacanth (n=135), or infected
with a single female cystacanth (n=143). A number
of isopods harboured 2 or more cystacanths (n=44).
These multiply infected isopods tended to be larger
than average (one-sample t-test against overall
mean isopod size, t43=4.54, P<0.0001). As the upper portion of the host size distribution was overrepresented, size by colouration correlations for
multiply infected isopods may not be comparable to
singly infected and uninfected isopods, so they were
excluded from the analysis. Also, the few isopods
harbouring small, uninfective parasites (n=11) were
excluded from the data.
The first and main statistical analysis compared
the colouration of uninfected and infected isopods
(split by worm sex). Both isopod body and abdominal
colouration were evaluated with ANCOVA. Infection status and isopod sex were fixed factors and
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isopod size was used as a covariate. Because isopods
were collected at different times and kept under
different lab conditions, an experimental ‘ block ’
factor was also included in the model (see Table 1).
Interactions between ‘ block ’ and other factors were
not assessed because of the low sample sizes for some
subgroups in some blocks (i.e. there were too few
female isopods, too few isopods with a male cystacanth, etc.). However, Benesh et al. (2009) found that
the effect of infection on colouration did not vary
with season or light/temperature treatment, suggesting that any interaction effects are weak. All other
interactions were initially included in the model.
Non-significant interactions were sequentially removed to reduce model complexity.
A second, subanalysis assessed whether parasite
size affects host colouration, and thus involved only
infected isopods. The most parsimonious ANCOVA
models (i.e. with non-significant interactions removed) from the first analysis were taken as a basis
for the second analysis. Parasite size was added as a
covariate to these base models and its main effect and
interaction effects were checked. This analysis,
therefore, assessed whether parasite size explains
any additional variation in isopod colouration not
covered by the main model.
Experimental infection and opercular colouration
To check the validity of the results obtained with
naturally infected isopods, colouration changes were
also observed in experimentally infected isopods.
Isopods were collected in August 2005 with a dipnet
from Niemijärvi, a small pond in central Finland
(62x12kN 25x45kE) in which the only fish species
present is Carassius carassius, the crucian carp. Thus,
all isopods were uninfected because the definitive
host of the parasite is not present in the pond.
Isopods were either exposed to fish faeces containing
parasite eggs or sham-exposed with distilled water
(the details of this infection have been reported by
Benesh and Valtonen (2007 a)). Isopods were observed for 101 days before any remaining animals
were killed and dissected. Nearly all exposed isopods
were infected with multiple parasites, and the number and size of all parasites were recorded from each
isopod. The average infection intensity for the isopods used in this analysis was 17.24 (S.D.¡8.35). For
most of the isopods that died 75 days or more postexposure, the respiratory operculae were collected
and stored in 70 % EtOH. Opercula were dehydrated
through an EtOH series, and then mounted, ventral
side up, on microscope slides in Euparal medium.
The opercula were photographed at 40r magnification using a Nikon Coolpix 4500 camera (scene
mode : close up, focal length : 96 mm, aperture : F5.4,
shutter speed : 1/500, sensitivity : ISO100, image
size : 1600r1200 pixels, image quality : fine, focus
mode : auto) attached to a light microscope with an
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D. P. Benesh, O. Seppälä and E. T. Valtonen
RESULTS
Host size – parasite size relationship
In natural infections, the relationship between
parasite volume and isopod size was dependent on
worm sex (ANCOVA, isopod sizerworm sex,
F1, 274=84.0, P<0.0001). In accordance with the
results of Benesh and Valtonen (2007 c), female cystacanth size increased more steeply with host size than
male size (Fig. 1A). The same pattern was observed
when parasite dry mass was used (ANCOVA, isopod
sizerworm sex, F1, 112=34.4, P<0.0001), although
the difference between males and females was not as
pronounced (Fig. 1B).
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1.6
A.
Females
Males
Cystacanth Volume
1.4
1.2
1.0
0.8
0.6
0.4
0.2
4.0
5.0
6.0
7.0
8.0
9.0
10.0
11.0
Isopod Length (mm)
0.40
B.
0.35
Cystacanth Dry Mass
M28r0.75 digital coupler (Thales Optem Inc.,
Fairport, NY, USA). Opercular colouration was
analysed in a similar manner as described above
for whole isopod photographs. Reflectance was
measured from a circular area (400-pixel diameter) in
the middle of both the left and right operculae, and
these values were averaged to give a mean reflectance
value for each isopod. A subsample of operculae was
photographed a second time to establish that the
method was repeatable (n=29, R=0.99, F28, 29=271,
P<0.001).
Opercular colouration for unexposed controls (n=
34) was compared to that of exposed, infected isopods (n=45) with a Mann-Whitney U-test. A multiple regression model was then used to examine how
the characteristics of the parasite infrapopulation
affected opercular colouration. The total worm volume harboured by an infected isopod was included as
a predictor. However, the distribution of parasite
volume among individuals may also be important,
i.e. pigment alteration may differ between a host with
a few large worms and one with several small worms.
In hosts harbouring a few big parasites, the average
volume of worms, relative to the total, should increase. Residuals were taken of a regression of average worm size on total worm size. These residuals
represent the variation in average worm size independent of the total parasite volume. For example,
positive residuals (a large average volume relative to
the total) characterize hosts in which the total parasite volume is concentrated into fewer individuals.
Using residuals as a measure of average worm size in
the regression model also circumvented the problem
of collinearity (Mason and Perreault, 1991). Because
A. lucii is sexually dimorphic, the sex ratio of the
infrapopulation may affect how worm volume is
distributed among individual parasites, so log sex
ratio was also included in the regression model. The
operculae from most infected isopods (77.8 %) were
collected 94–101 days post-exposure, so parasite age
varied little and was not included in the model.
All statistical analyses were performed with SPSS
14.0 (SPSS Inc., Chicago, Illinois) software.
Females
Males
0.30
0.25
0.20
0.15
0.10
0.05
0.00
4.0
5.0
6.0
7.0
8.0
9.0
10.0
11.0
Isopod Length (mm)
Fig. 1. The relationship between isopod size and parasite
size measured as (A) volume (mm3) or as (B) dry mass
(mg). Male and female cystacanths came from singly
infected isopods collected from the field.
Isopod colouration in naturally collected isopods
After removing non-significant interactions, the
terms included in the ANCOVAs were identical for
body and abdominal coloration (from here BC and
AC, respectively ; Table 2). For both BC and AC,
there was a significant interaction between infection
status and isopod size (F2, 609=4.14, P=0.016 and
F2, 609=8.21, P<0.001, respectively; Table 2). This
is a violation of the ‘ homogeneity of regressions ’
assumption of ANCOVA, i.e. the relationship between the dependent variable (colouration) and the
covariate (isopod size) differs among levels of the
factor (infection status). Consequently, the estimated
main effect of infection status may be biased. Thus,
uninfected, male-infected, and female-infected isopods are only compared within the context of isopod
size. The slope of the BC by size relationship was
steepest for isopods infected with a female cystacanth, but the between-group differences were small
(Fig. 2A). The interaction was clearer for AC. The
difference between infected and uninfected isopods
increased with isopod size, because the AC of
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Larval size and host colouration
Table 2. Summary of ANCOVA analyses
evaluating isopod colouration
100
D.F.
5.77
19.70
23.33
143.54
4.14
32.57
2
1
8
1
2
1
609
0.003
<0.001
<0.001
<0.001
0.016
<0.001
2
1
8
1
2
1
609
<0.001
0.004
<0.001
<0.001
<0.001
0.001
8.28
8.37
20.10
89.59
8.21
11.21
P
80
70
60
less than 6
6 to 7
7 to 8
8 to 9
9 to 10 more than 10
Isopod length (mm)
90
B.
Uninfected
Female cystacanth
Male cystacanth
80
Abdominal Coloration
Body colouration
Infection status
Isopod sex
Block
Isopod size
Infection statusrIsopod size
Isopod sexrIsopod size
Error
Abdominal colouration
Infection status
Isopod sex
Block
Isopod size
Infection statusrIsopod size
Isopod sexrIsopod size
Error
F
Uninfected
Female cystacanth
Male cystacanth
90
Body Coloration
(Isopods were classified as uninfected, infected with a male
cystacanth, or infected with a female cystacanth. The block
factor refers to the different experimental treatments listed
in Table 1. Non-significant interaction terms (P>0.05)
were sequentially removed from the ANCOVAs to produce more parsimonious models.)
A.
70
60
50
infected isopods became conspicuously darker in
larger isopods (Fig. 2B). There was also a difference
between worm sexes. Small isopods infected with a
male cystacanth tended to have darker AC than those
infected with a female cystacanth, but in larger isopods AC was similar (Fig. 2B). For BC and AC, there
was a significant interaction between isopod sex and
size (Table 2), because female isopods were slightly
darker than males when large but not when small.
Adding parasite size to the ANCOVAs, either as
volume or mass, did not produce any new results.
For both AC and BC, worm size and all its interactions were non-significant (all P>0.05), indicating
that parasite size did not explain any additional variation in host colouration beyond that described in the
main analysis.
Opercular colouration in experimentally
infected isopods
The operculae of exposed, infected isopods were
darker than those of control isopods (Mann-Whitney
U-test, Z=x5.13, P<0.001). Hosts harbouring a
larger total parasite volume tended to have darker
operculae (standardized beta=x0.39, t41=x3.02,
P=0.004 ; Fig. 3A). Moreover, a large average worm
volume, relative to the total, was also associated with
darker operculae (standardized beta=x0.41, t41=
x3.20, P=0.003 ; Fig. 3B), which suggests that
isopods with a few large worms had more severely
altered pigmentation than those with many small
worms. The infrapopulation sex ratio did not affect
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less than 6
6 to 7
7 to 8
8 to 9
9 to 10 more than 10
Isopod length (mm)
Fig. 2. Body (A) and abdominal (B) colouration as a
function of isopod length. The data are separated into
uninfected isopods (circles, solid line), isopods infected
with a single female cystacanth (open triangles, dashed
line), and isopods infected with a single male cystacanth
(open squares, broken line). Statistical analyses treated
isopod size as a continuous variable, but trends were
difficult to discern in a scatter-plot due to the extensive
overlap among individual data points. Thus, for clarity,
isopod size is plotted as a categorical variable.
Colouration is lighter at higher values on the scale.
Bars represent the 95% CI.
opercular colouration (standardized beta=x0.05,
t41=x0.35, P=0.73).
DISCUSSION
The alteration of isopod colouration only occurs after
parasites become cystacanths (Brattey, 1983). However, maximum host alteration was not achieved
immediately after attaining the cystacanth stage. In
both naturally and experimentally infected isopods,
larger parasites more strongly altered host pigmentation. In the naturally infected isopods, abdominal
colouration was darkest, relative to uninfected isopods, in large hosts that harboured bigger worms.
Likewise, a large total parasite volume was associated
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D. P. Benesh, O. Seppälä and E. T. Valtonen
A.
Opercular Coloration
210
180
150
120
90
0.0
2.5
5.0
7.5
10.0
12.5
Total Worm Volume
B.
Opercular Coloration
210
180
150
120
90
-0.4
-0.2
0.0
0.2
0.4
0.6
Average Worm Volume Relative to Total
Fig. 3. The relationship between opercular coloration
and (A) the total parasite volume (mm3) harboured by
experimentally infected isopods and (B) the residuals
of a regression of average parasite volume against total
parasite volume. Positive residuals represent hosts with
a large average parasite volume relative to the total,
i.e. the total parasite volume is concentrated into fewer
individuals. The solid lines are the least squares
regression lines for the data, while the dashed lines
represent the mean opercular colouration of unexposed,
control isopods. Colouration is lighter at higher values on
the scale.
with darker opercular colouration in experimentally
infected isopods, particularly when it was distributed
among fewer individual worms. Moreover, the experimental isopods were sampled at about the same
time, so the relationship between parasite size and
host colouration was not confounded by potential
effects of parasite age. Parasite age might also influence host manipulation, but we could not assess this,
as there was little variation in parasite age in our experimental data. Evaluating the relative importance
of parasite size versus age requires independent
variation in each, e.g. parasites could be sampled at
different ages after they had been growing at different
rates.
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Though larger, more modified hosts harboured
larger parasites, parasite size was not a significant
covariate in the ANCOVA analyses conducted with
the field-collected isopods. This was probably because parasite size did not explain any additional
variation in colouration beyond that described by
host size. That is, parasites that were large (or small)
relative to their host’s size did not modify host pigmentation more (or less) extensively. Modification of
other host traits may also increase as parasites grow,
though imperfectly. For example, from late summer
to the following spring, the size of isopods and parasites increases, as does the alteration of host hiding
behaviour (Benesh et al. 2009). However, host behaviour is not clearly modified in late autumn, even
though isopods are of a similar size to those collected
in spring (Benesh et al. 2009). Thus, for both host
behaviour and colouration, there is a positive, but
imperfect correlation between parasite size and trait
alteration. Similar trends have been noted in tapeworms in their fish second intermediate hosts. For
example, Brown et al. (2001) found that fish infected
with larger Ligula intestinalis plerocercoids had more
altered habitat choice, and Ness and Foster (1999)
found larger Schistocephalus solidus in demelanized
sticklebacks. Size-dependent manipulation may be an
adaptive strategy, because, as parasites grow larger,
the relative benefits of remaining in the intermediate
host decrease while the potential costs increase. At
some point, the amount of additional larval growth
possible diminishes due to space or resource constraints (Michaud et al. 2006 ; Benesh and Valtonen,
2007 b; Shostak et al. 2008). Concomitantly, the
probability of natural host mortality presumably
increases. Therefore, the profitability of transmission, and by association host manipulation, is
likely to increase as parasites grow over time.
Many acanthocephalans are sexually dimorphic as
cystacanths (e.g. Amin et al. 1980 ; Oetinger and
Nickol, 1981 ; Steinauer and Nickol, 2003), presumably because the benefits of a large larval size are
more pronounced for females than males (Benesh
and Valtonen, 2007 c). This sexual dimorphism
might favour divergent manipulation strategies.
Oetinger and Nickol (1981), however, did not observe differences in the ‘‘ pigment dystrophy ’’ exhibited by isopods infected with male or female
Acanthocephalus dirus cystacanths. The hiding behaviour of isopods infected with a male or female
A. lucii cystacanth also does not seem to differ
(Benesh, unpublished data). In this study, male
worms appeared to alter isopod abdominal colouration more extensively than female worms in small
hosts, but in larger hosts this difference disappeared.
Because female cystacanth size increases rapidly with
host size, females in small hosts may have more
to gain than males by remaining in and growing
mutually with the host (infection does not impair
isopod growth, Benesh and Valtonen, 2007 a ; Hasu
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Larval size and host colouration
et al. 2007). The more extensive modification of
small hosts by male parasites may thus reflect their
relatively higher incentive to be transmitted. By
contrast, in larger isopods, neither male nor female
parasites may profit from staying in the intermediate
host, favouring similar, high levels of host modification by both sexes. Sexually divergent manipulation strategies could also arise via differences in
resource availability, assuming manipulation entails
energetic costs. Because male parasites invest less
in growth, they may have more resources available
to allocate toward modifying host pigmentation.
However, the largest colouration difference between
male- and female-cystacanth infections was observed
in small isopods when parasite size dimorphism is
relatively low and resource pools are presumably
similar. This suggests that the sex-specific manipulation strategies stem from different optimal sizes for
transmission rather than dissimilarities in resource
availability.
Visual-based predation by fish is likely to be a
selective force maintaining cryptic colouration in
A. aquaticus (Hargeby et al. 2004, 2005), so the
conspicuously darker abdominal pigmentation of
naturally infected isopods probably increases their
susceptibility to predation by fish definitive hosts
(Brattey, 1983 ; Seppälä et al. 2008). If large heavily
manipulated hosts harbouring large parasites are
taken more easily by predators, then parasite abundance may be higher in hosts of medium size. Consistent with this prediction, natural A. lucii
abundance peaks in intermediate-sized isopods and
is reduced in large isopods (Brattey, 1986). Although
a number of processes can produce this pattern (e.g.
age-dependent exposure, Duerr et al. 2003), it would
be interesting to see if other helminths with similar
distributions in their intermediate host populations
(Thomas et al. 1995 ; Rousset et al. 1996 ; Outreman
et al. 2007) also increase host manipulation as they
grow. Unlike A. lucii, however, many parasites
exhibit relatively fixed growth strategies, i.e. after
developing to an infective stage, growth stops. For
these species, there may be no additional benefits,
only costs, associated with remaining in the intermediate host after infectivity is reached, so discrete
changes in the level of host manipulation might be
favoured. Different parasite growth patterns may,
thus, lead to different host manipulation strategies.
Jukka Jokela and two reviewers gave helpful comments on
an earlier version of this manuscript. D.P.B. was supported
by the Biological Interactions Graduate School at the
University of Turku and O.S. by the Academy of Finland.
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