International Journal for Parasitology 35 (2005) 137–143
www.parasitology-online.com
Parasites grow larger in faster growing fish hosts
Iain Barbera,b,*
a
Institute of Biological Sciences, University of Wales Aberystwyth, Edward Llwyd Building, Penglais Campus, Aberystwyth,
Ceredigion SY23 3DA, Wales, UK
b
Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow, Scotland, UK
Received 20 August 2004; received in revised form 8 November 2004; accepted 12 November 2004
Abstract
Parasites depend on host-derived energy for growth and development, and so are potentially affected by the host’s ability to acquire
nutrients under competitive foraging scenarios. Although parasites might be expected to grow faster in hosts that are better at acquiring
nutrients from natural ecosystems, it is also possible that the most competitive hosts are better at countering infections, if they have an
improved immune response or are able to limit the availability of nutrients to parasites. I first quantified the ability of uninfected three-spined
sticklebacks Gasterosteus aculeatus to compete in groups for sequentially-presented food items, and then exposed either the best or worst
competitors to infective stages of the cestode Schistocephalus solidus. Fish were subsequently raised in their original groups, under
competitive feeding regimes, for 96 days, after which fish and parasite growth was determined. Unexpectedly, pre-exposure host competitive
ability had no effect on susceptibility to infection, or on post-infection growth rate. Furthermore, despite a 120-fold variation in parasite mass
at the end of the study, pre-infection competitive ability was not related to parasite growth. The closest predictor of parasite mass was body
size-corrected host growth rate, indicating that the fastest growing fish developed the largest parasites. Faster growing hosts therefore
apparently provide ideal environments for growing parasites. This finding has important implications for ecology and aquaculture.
q 2004 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.
Keywords: Stickleback; Schistocephalus solidus; Competitive ability; Fitness; Host–parasite relationships; Growth
1. Introduction
Within populations, individuals differ in their ability to
compete for limited resources (Begon et al., 1990) and the
resulting unequal division of nutrients leads to variation in
growth rates, body size and nutritional condition (e.g.
Rubenstein, 1981; Metcalfe, 1986; Westerberg et al., 2004).
Unequal nutrient intake by competitors is also likely to have
consequences for any parasites they may harbour, though it
is difficult to predict the direction of such effects. On the one
hand, because parasites are completely dependent on hostderived energy for growth and development (Bush et al.,
2001), infecting better competitors might benefit parasites,
particularly those with significant energetic requirements.
* Address: Institute of Biological Sciences, The University of Wales
Aberystwyth, Edward Llwyd Building, Penglais Campus, Aberystwyth,
Ceredigion SY23 3DA, Wales, UK. Tel.: C44 1970 622320; fax: C44
1970 622350.
E-mail address: [email protected]
Alternatively, if the best competitors are either in better
nutritional condition as a result of their competitive
superiority, or of intrinsically higher genetic quality, then
they may be poor hosts for parasites if they have better
immune systems or are able to limit the availability of
nutrients to growing parasites. Pre-existing variation in the
competitive ability of hosts therefore has potentially
important implications for parasite infections, but to date
no studies have directly tested this.
There is clear evidence from studies of parasitoids
(insects with parasitic larvae that feed on the bodies of other
arthropods, eventually killing them; Godfray, 1994) that
intraspecific variation in host body size and nutritional
status, which are likely correlates of competitive ability, can
affect parasite growth (e.g. Harvey et al., 1995; Otto and
Mackauer, 1998; Paine et al., 2004). If variation in body size
and nutritional condition reflects the prior competitive
foraging ability of parasitoid hosts these results might
suggest that better competitors make the best hosts for
parasites. Yet whether the results from parasitoid studies are
0020-7519/$30.00 q 2004 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.ijpara.2004.11.010
138
I. Barber / International Journal for Parasitology 35 (2005) 137–143
likely to apply to all host–parasite systems, particularly to
those involving vertebrate hosts, is questionable. Firstly,
although insect hosts are capable of mounting cellular
defences against parasitoids (e.g. Strand and Pech, 1995;
Kraaijeveld and Godfray, 1997) their antiparasite responses
are far less well developed than those higher animals
(Wakelin, 1996). Second, unlike parasitoids, the growth
stages of ‘true’ parasites do not generally kill their host,
being forced to sequester nutrients from living hosts. Given
these significant differences, it is important to test whether
host competitive ability mediates parasite success in a
vertebrate host that has greater potential to control
infections.
There is evidence that infection with nutritionally
demanding parasites can be associated with altered host
foraging strategies, including exploiting risky foraging
habitats, altering prey preferences and altering time budgets
in order to maximise food intake rates (e.g. Milinski, 1985;
Godin and Sproul, 1988; Ranta, 1995). Although
behavioural changes associated with infection may allow
infected hosts to maximise nutrient intake (Milinski, 1990),
it is not clear whether this benefits hosts or parasites, and
hence whether changes in host foraging behaviour are host
or parasite adaptations (Poulin, 1998). Examining the
relationship between the growth rates of hosts and their
parasites under competitive feeding conditions can provide
insight. If increased food intake benefits hosts by allowing
them to mount an immune response or otherwise limit
parasite growth a negative relationship between host and
parasite growth would be predicted. Conversely, a positive
relationship between host and parasite growth rates under
competitive foraging regimes would indicate that parasites
benefit from increased nutrient intake of hosts. The absence
of studies examining growth rates of hosts and their
parasites under competitive foraging conditions means
that the consequences of host competitive ability and of
infection-associated changes in host nutrient intake for host
and parasite fitness remain unknown.
Here, I examine how pre-existing variation in the
competitive ability of three-spined sticklebacks
Gasterosteus aculeatus affects the growth of the parasitic
cestode Schistocephalus solidus following experimental
infection, and investigate the relationship between host and
parasite growth over a 96-day period of food competition.
Schistocephalus plerocercoids are common parasites of
sticklebacks (Wootton, 1976), which become infected when
they eat copepods harbouring infective procercoids.
Plerocercoids grow rapidly in the stickleback body cavity,
imposing significant energetic demands, and ultimately
contribute up to 50% of the infected fish’s mass (Arme and
Owen, 1967). Schistocephalus can only achieve sexual
maturity in the intestine of an endotherm (generally a bird,
Smyth, 1985), relying on ingestion of the fish host for
transmission. The relative ease with which fish can be
experimentally infected, coupled with straightforward host
maintenance, makes this an ideal model system for
examining host–parasite interactions.
2. Materials and methods
2.1. Husbandry
Sexually mature sticklebacks hand-netted from
Inverleith Pond, Edinburgh UK (55855 0 N, 03810 0 W) in
June 1999 were allowed to spawn in aquaria at Glasgow
University, and embryos recovered from nests were
incubated until hatching (Barber and Arnott, 2000).
After 12 weeks of being fed an ad libitum diet of
Liquifrye, Artemia nauplii and bloodworms (Chironomus
sp. larvae), 19 groups of six, size-matched juveniles were
selected and each group transferred to a 40!20!20 cm
(16 L) aquarium. Group members were measured
(standard length, SL0, to 1 mm), weighed (wet weight,
W0, to 0.001 g) and marked with coloured plastic tags
attached to the second dorsal spine (Barber and Ruxton,
2000; tag colours did not include red or orange, colours
known to elicit aggressive attacks; Rowland, 1994). Mean
group SL0 ranged from 30.2 to 37.7 mm, and withingroup size range was always less than G10% of the mean
group SL0. Aquaria were provided with a gravel
substratum and a plastic plant for shelter; water was
maintained at 17G1 8C, filtered and aerated with sponge
airlift filters and partially replaced on a weekly basis. A
lighting regime of 14 h dark:10 h light was used.
2.2. Assigning competitive rank within groups
The relative competitive ability of individual fish in
each group was assessed by scoring foraging success in
three trials, undertaken on alternate days in December
1999 (d0, d2 and d4). During each trial, 20 bloodworms
were introduced to each tank at 5 min intervals, by pipette
via a suspended plastic funnel, and the identity of the fish
ingesting each prey item was recorded. A screen, fitted
with viewing windows, isolated the fish visually from the
observer. The proportion of items ingested by each fish on
each day was used to rank fish with respect to their
competitive ability within the group, generating three
daily performance ranks (Rd0, Rd2, Rd4) that were
averaged to give a mean rank (Rm). This was then used
to assign each fish an overall rank (R) from 1 (best
competitor) through 6 (worst competitor) in its group.
Where tied Rms were generated, the fish that ingested the
most prey items over all three trials was assigned the
more competitive R value.
2.3. Parasite exposure
Infected copepods were generated by exposing individuals to infective coracidia and scoring the number of visible
I. Barber / International Journal for Parasitology 35 (2005) 137–143
procercoids after 6 and 27 days. Either the best two
competitors (ranked 1 and 2 in the group), or the worst
two competitors (ranked 5 and 6), from each group were
placed in separate 50 ml glass dishes filled with water and
presented with an experimentally-infected cyclopoid
copepod harbouring at least one infective S. solidus
procercoid. Each fish was observed until it ingested the
infected copepod (see Arnott et al., 2000 for detailed
parasite culture and infection details). All parasites
emanated from one, self-fertilised adult worm. Copepod
screening confirmed that all ‘infected’ copepods contained
at least a single infective procercoid, but in some cases
multiply infected copepods were unintentionally fed to the
fish (see Results).
139
and
HSIðinfÞ Z ðWliver =ðW96 K TPWÞÞ !100:
(5)
3. Results
3.1. Competitive asymmetry between group members
Fig. 1a shows the proportion of food items ingested by
the six fish in each group, ranked by performance in each of
the daily screening trials. The best competitors ingested a
mean of 38.3% of food items, and the worst competitors
only 2.9%; equal shares would have given each fish 16.7%
2.4. Growth, hepatosomatic index and parasite load
After being fed infective parasites, exposed sticklebacks
were returned to their original groups, which were provided
daily with bloodworms, ad libitum by pipette, over a 96-day
period. Although the daily ration was not quantified, at each
feeding sufficient bloodworms were provided to allow all
fish to feed, but input ceased before any of the fish stopped
responding to the incoming food. Thus all fish were
constantly motivated to feed, and a high level of food
competition was maintained in the tanks. At the termination
of the study, all fish were measured (SL96, to 1 mm) and
weighed (W96, to 0.001 g) before being dissected to confirm
infection status and sex. The liver was dissected from each
fish and weighed (to 0.001 g). For each experimentally
infected fish, the number and weight (to 0.001 g) of all
plerocercoids recovered from the body cavity were
recorded, allowing the calculation of total plerocercoid
weight (TPW) and parasite index (PI, Arme and Owen,
1967):
PI Z ðTPW=W96 Þ !100:
(1)
The specific growth rate (SGR) achieved by each fish
over the 96-day period, and its terminal hepatosomatic
index (HSI, an indicator of energy reserves; Chellappa et al.,
1995), was then calculated. SGR for non-infected fish was
calculated using the equation
SGR Z 100 !ððln W96 Þ K ðln W0 Þ=96Þ
(2)
and HSI was calculated for non-infected fish using the
equation:
HSI Z ðWliver =W96 Þ !100:
(3)
To calculate SGR and HSI for infected fish, it was first
necessary to subtract plerocercoid weight from terminal
weight. Hence equations used to calculate SGR and HSI for
infected fish were
SGRðinfÞ Z 100 !ððlnðW96 K TPWÞÞ K ðln W0 Þ=96Þ
(4)
Fig. 1. The distribution of food items between competing sticklebacks in
groups of six in feeding competition trials. (a) The proportion of food items
taken by fish within groups, ranked by their performance on each day.
(b) The proportion of food taken on three alternate days by fish ranked by
their overall position in the group; different letters identify statistically
significant differences between groups (P!0.05, see text for details). Bar
heights are means; error bars represent one SD. Broken horizontal lines
show the proportion expected if fish ingested an equal share (nZ19 groups).
140
I. Barber / International Journal for Parasitology 35 (2005) 137–143
of the food. The performance of individuals within groups
was consistent over the three pre-exposure trials, and this is
evidenced by Fig. 1b, which shows the mean proportion of
items taken across all three trials by those fish ranked as first
through sixth overall. The proportion of available food
taken by the fish ranked as 1–2, 3–4, and 5–6 differed
significantly from each other (ANOVA: F2,110Z98.04,
P!0.0001; all comparisons P!0.05; Fig. 1b).
3.2. Mortality
Mortality was low, with only 18 of the 114 fish dying
before the end of the 96-day study. Losses were largely
restricted to four groups, from which a total of 12 fish died at
early stage, before infection status could be ascertained.
These groups were removed from the analysis. Six other
groups, each of which lost a single fish, were retained in the
analysis. Of the six fish that died from these groups, none
had been exposed to infective stages of S. solidus.
3.3. Infection susceptibility: effects of host body size
and competitive ability
Plerocercoids were recovered from 24 of the 30 surviving
fish fed infected copepods. There was no detectable effect of
initial body size on infection susceptibility, with the six
exposed-uninfected fish being spread across the spectrum of
body sizes. Pre-exposure competitive ability was not
important in determining susceptibility, with infections
being just as likely to develop in poor competitors as in good
ones (10/14 exposed good competitors developed infections
compared to 14/16 exposed poor competitors; c2Z1.21,
dfZ1, PZ0.27). Sixteen of the experimentally infected fish
harboured a single plerocercoid, with the remainder
harbouring multiple infections (three with two
plerocercoids; one with three; one with four; two with
five; one with eight). Multiple infections, which arise
through imperfect copepod screening procedures
(Arnott et al., 2000), were not associated with significantly
different infection profiles compared with single infections
(Wilcoxon–Mann–Whitney test: TPW, W16,8Z220.5,
PZ0.22; PI, W16,8Z211.0, PZ0.52), so data for all
infections were combined.
3.4. Host growth: effects of initial body size and
competitive ability
As expected, host SGR was inversely related to initial
body weight (SGRZK1.67[W 0]C0.75, F1,23Z5.53,
PZ0.028), so residual SGR values (rSGR) were calculated
to correct growth rates for initial body size. Pre-exposure
competitive ability did not affect the post-infection rSGR of
host sticklebacks (Kruskall–Wallis ANOVA, H10,14Z0.17,
PZ0.68; Fig. 2a).
3.5. Parasite growth: effects of initial host competitive
ability and post-infection host growth
At autopsy TPW ranged from 0.001 to 0.120 g
(meanGSD: 0.038G0.027 g), contributing PIs of between
0.4 and 20% (meanGSD: 9.1G5.0%) of the mass of
infected fish. Pre-infection competitive ability had no effect
on either TPW or PI (Wilcoxon–Mann–Whitney test: TPW:
Fig. 2. The lack of effect of pre-infection competitive ability on the growth performance of hosts sticklebacks and their parasites at autopsy, 96 days
post-infection (a) The body size-corrected specific growth rate (b) the total plerocercoid weight and c) the parasite index of host sticklebacks that were the worst
and best competitors in groups, prior to parasite infection. Bar heights are means; error bars represent one SD.
I. Barber / International Journal for Parasitology 35 (2005) 137–143
141
The HSI of males was not significantly affected by infection
(H 23,5Z1.18, PZ0.28), though not enough groups
contained both infected and non-infected males to allow a
group level analysis.
4. Discussion
Fig. 3. The relationship between total parasite weight and the body-size
corrected growth rates of sticklebacks over the 96-day post-infection
period. Filled circles represent those fish ranked as the best competitors in
groups, and open triangles represent the worst competitors in groups, prior
to parasite infection.
W10,14Z116.0, PZ0.62; PI: W10,14Z120.0, PZ0.79;
Fig. 2b and c), with initially poor and good competitors
being capable of sustaining the growth of the heaviest
infections.
Initial host weight did not influence TPW (F1,23Z2.44,
PZ0.133) but there was a highly significant positive
relationship between final host weight and TPW
(F1,23Z13.45,
PZ0.001).
Host
weight
gain
((W96KTPW)KW0) also predicted TPW (F1,23Z6.14,
PZ0.021), but the specific growth rate of the host, after
correction for initial body size, was more closely related to
TPW (F1,23Z9.41, PZ0.006; Fig. 3). The relationships
between host rSGR and plerocercoid weight for initially
poor and good competitors did not differ (Analysis of
covariance (ANCOVA), slope, F1,23Z3.22, PZ0.088;
elevation, F1,23Z0.42, PZ0.52).
3.6. Effects of parasite infection on hepatosomatic
index (HSI)
Combining data from all groups, there was a clear effect
of infection status on female HSI, with infected females
having considerably smaller livers for their body size
(Kruskall–Wallis ANOVA, H 41,19Z6.79, PZ0.009).
Analysing the data by group confirmed this general pattern;
in groups containing both infected and non-infected
females, the mean HSI of uninfected females was
significantly higher that of infected females (Wilcoxon
signed rank test; WZ42.0, nZ9 groups, PZ0.024).
In this study, juvenile sticklebacks showed repeatable
variation in their ability to compete for food in groups,
allowing competitive rank to be identified unambiguously.
Variation in pre-exposure competitive ability was not
related to infection susceptibility, and S. solidus was equally
likely to establish in the best as in the worst competitors.
Furthermore, the growth of hosts post-infection was
unrelated to their pre-infection competitive ability. Moreover, although the plerocercoid weight harboured by
infected fish at the end of the study showed a 120-fold
variation, it was not affected by the host’s pre-exposure
competitive ability. The closest predictor of plerocercoid
weight was the specific growth rate attained by the fish host
during the infection period, corrected for initial body size,
demonstrating that, under competition for limited food
resources, host and parasite growth rates are positively
linked, with faster growing hosts providing better environments for parasite growth. A robust, significant negative
impact of infection on the energy reserves of female
sticklebacks was also detected.
Eighty percent of all exposed sticklebacks developed
infections in the study, with both poor and good competitors
being equally likely to become infected following exposure.
Such high infectivity is comparable with other experimental
studies of S. solidus (e.g. Barber et al., 2001; Christen and
Milinski, 2003). Yet although host competitive ability
appears not to affect parasite resistance, it may be important
in determining patterns of infection if the best competitors
are less exposed to infection because they are able to select
high quality (non-parasitised) prey (Wedekind and Milinski,
1996). One explanation for the general lack of effect of preexposure infection status on either host or parasite growth
could be that infections changed the competitive feeding
behaviour of stickleback hosts and dramatically altered the
competitive dynamics of the groups. Although this study did
not test directly for infection-associated behaviour changes,
S. solidus infections are known to be associated with
increased host foraging effort (e.g. Milinski, 1985; Godin
and Sproul, 1988; Barber and Ruxton, 1998), presumably to
compensate for the combined pressures of infectionassociated disability and increased nutrient requirements
(Milinski, 1990). It is possible that under competitive
foraging situations, infections have opposite effects on the
nutrient intake of the best and worst competitors; previously
poor competitors may become more competitive, but the
best competitors may fail to maintain dominant feeding
positions because of the debilitating effects of infection (see
also Gourbal et al., 2002). The combined effects of
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I. Barber / International Journal for Parasitology 35 (2005) 137–143
increased motivation and reduced ability associated with
infection may therefore have the effect of standardising the
competitive ability of previously good and poor
competitors.
Amongst fish that developed infections, there was a
120-fold variation in TPW and a 50-fold variation in PI after
96 days. Since the progeny of a single, selfed parasite was
used to infect sticklebacks, observed parasite growth
variation was most likely due to differential host responses
to infection. Because parasite growth was unrelated to initial
host competitive ability, neither the hypothesis that better
competitors are better equipped to deal with infections, nor
the hypothesis that better competitors are better hosts
for parasites because they reduce nutrient limitations on
parasite growth, are supported. Infection-associated changes
in the competitive feeding behaviour of fish may therefore be
more important in determining the flow of nutrients to the
host–parasite system than pre-exposure differences in initial
competitive ability. An important finding was that hosts
achieving the highest growth rates post-infection developed
the largest plerocercoid burdens. This result provides an
explanation for the finding of Aeschlimann et al. (2000) that,
during early infection, sticklebacks did not exploit competitor-free risky foraging opportunities to ‘outgrow’ the
parasite, as had been expected. The results of the present
study suggest that infected fish are incapable of countering
infections by investing in rapid somatic growth, since host
growth can only be achieved with a concomitant increase in
plerocercoid growth. This experimentally-derived result
supports a recent demonstration that host and plerocercoid
body sizes co-vary within a single age-cohort of sticklebacks
from Walby and Scout lakes, Alaska (Heins et al., 2002).
Further studies should investigate the generality of this
finding, which may have important implications
for aquaculture, where techniques adopted to maximise fish
growth rates could have concomitant effects on parasite load.
Although S. solidus plerocercoids smaller than 50 mg can
mature in vivo (Clarke, 1953; Hopkins and McCaig, 1963),
plerocercoids only become reliably infective to definitive
hosts at a mass exceeding this size (Tierney and Crompton,
1992). Plerocercoids reaching 50 mg more quickly therefore
reduce the risk of non-transmission following the premature
death or predation of their host. Furthermore, for plerocercoids exceeding 50 mg, body size is related positively to
adult fecundity and egg size (Wedekind et al., 1998;
I. Barber, D. Wilson and M. Dörücü, unpublished data),
meaning that plerocercoids achieving a larger size before
transmission to the definitive host produce more eggs as
adults. In this study, five of the 11 infected fast-growing hosts
(i.e. with positive rSGRs; ranked 3rd, 6th, 9th, 10th and 11th
in growth out of the total of 24 infected fish) harboured a
plerocercoid mass O50 mg within the 96-day study period,
compared to just one of the 13 slow-growing hosts (ranked
20th out of 24). The increased growth attained by parasites in
faster-growing hosts therefore has significant fitness
implications.
In studies examining the energetics of fish host–parasite
relationships, hosts are typically fed individually, under
non-competitive conditions (Barber and Svensson, 2003;
Christen and Milinski, 2003). Such studies allow individual
intake rates to be investigated, but unnaturally favourable
husbandry conditions can mask ecologically relevant effects
of infection (Candolin and Voigt, 2001). Under competitive
foraging conditions in this study, infected females developed smaller livers than uninfected females. This supports
field data suggesting that infections impose significant
energetic costs (e.g. Arme and Owen, 1967; Pennycuick,
1971; Tierney et al., 1996; Bagamian et al., 2004), whereas
studies examining fish held under more favourable conditions can fail to show such effects (e.g. Arnott et al., 2000;
Barber and Svensson, 2003). Studies where parasitised fish
are fed individually (e.g. Barber and Svensson, 2003; Kurtz
et al., 2004) also generate less variably-sized plerocercoid
burdens than found here. To generate data that are more
applicable to natural field situations, it is necessary to raise
infected fish in competitive groups, and this has
implications for future study design.
The factors controlling the growth of helminth parasites in
their hosts are of current interest. Parker et al. (2003) suggest
that the size attained by larval cestodes may reflect either
host-imposed resource constraints on growth, or arise as a
result of evolved life history strategies. Experimental data
presented in their paper suggest that the growth patterns of
S. solidus in multiply-infected copepods appear to support
the energetic constraints model. The observed growth of
S. solidus plerocercoids in stickleback hosts in the present
study is also consistent with the view that the growth is
limited by host resources. Plerocercoid growth rate may also
be related to the diversity of the host’s major histocompatibility complex (Mhc), with hosts possessing too few or too
many Mhc alleles developing larger plerocercoids than those
with intermediate Mhc diversity (Milinski, 2003; Kurtz et al.,
2004). Further studies examining the interaction between
host nutrient intake, Mhc diversity and parasite growth,
carried out under ecologically relevant competitive regimes,
are required to fully understand the factors that generate
intra-population variation in parasite load.
Acknowledgements
IB was supported by NERC postdoctoral research
fellowships (GT/5/98/6/FS and NER/I/S/2000/00971).
Fish were experimentally infected and maintained in
accordance with local and national welfare guidelines,
under UK Home Office Project Licence 60/2025. Thanks to
the Glasgow Fish Biology Group and the UWA Parasitology
Group for stimulating discussion, and to John Laurie,
Raellie Paterson and Hazel Wright for fish husbandry
assistance.
I. Barber / International Journal for Parasitology 35 (2005) 137–143
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