Journal of Animal Ecology 2011, 80, 990–998
doi: 10.1111/j.1365-2656.2011.01834.x
Introduced brown trout alter native acanthocephalan
infections in native fish
Rachel A. Paterson1*, Colin R. Townsend1, Robert Poulin1 and Daniel M. Tompkins2
1
Department of Zoology, University of Otago, PO Box 56, Dunedin 9054, New Zealand; and 2Landcare Research, Private
Bag 1930, Dunedin 9054, New Zealand
Summary
1. Native parasite acquisition provides introduced species with the potential to modify native
host–parasite dynamics by acting as parasite reservoirs (with the ‘spillback’ of infection increasing
the parasite burdens of native hosts) or sinks (with the ‘dilution’ of infection decreasing the parasite
burdens of native hosts) of infection.
2. In New Zealand, negative correlations between the presence of introduced brown trout (Salmo
trutta) and native parasite burdens of the native roundhead galaxias (Galaxias anomalus) have
been observed, suggesting that parasite dilution is occurring.
3. We used a multiple-scale approach combining field observations, experimental infections and
dynamic population modelling to investigate whether native Acanthocephalus galaxii acquisition
by brown trout alters host–parasite dynamics in native roundhead galaxias.
4. Field observations demonstrated higher infection intensity in introduced trout than in native
galaxias, but only small, immature A. galaxii were present in trout. Experimental infections also
demonstrated that A. galaxii does not mature in trout, although parasite establishment and initial
growth were similar in the two hosts. Taken together, these results support the hypothesis that
trout may serve as an infection sink for the native parasite.
5. However, dynamic population modelling predicts that A. galaxii infections in native galaxias
should at most only be slightly reduced by dilution in the presence of trout. Rather, model exploration indicates parasite densities in galaxias are highly sensitive to galaxias predation on infected
amphipods, and to relative abundances of galaxias and trout. Hence, trout presence may instead
reduce parasite burdens in galaxias by either reducing galaxias density or by altering galaxias
foraging behaviour.
Key-words: dilution effect, disease, galaxias, introduced species, New Zealand, parasite,
salmonid
Introduction
Introduced species have the potential to modify native host–
parasite dynamics through the acquisition of native parasites.
Recent reviews have demonstrated that introduced animals
may acquire about five native parasites on average, with
some gaining more than 16 (Torchin et al. 2003; Kelly et al.
2009b). These reviews highlight that not only do a great variety of introduced species acquire native parasites, but also
that the acquired parasites are highly diverse.
The frequency with which introduced species acquire
native parasites has led to increasing attention to the ways
they can modify native parasite dynamics. Parasite ‘spillback’
to a native host may result from the acquisition of native parasites by an introduced species, provided that it becomes a
*Correspondence author. E-mail: patra374@student.otago.ac.nz
competent host that can act as a reservoir of infection
(Daszak, Cunningham & Hyatt 2000; Tompkins & Poulin
2006; Kelly et al. 2009b). The spillback of parasites may act
as an additional threat to native biodiversity via increased
disease impacts on species already facing mounting pressures
from other sources such as competition, predation, habitat
loss, pollution and climate change. Recent studies have also
documented how the acquisition of native parasites by introduced species may lead to parasite ‘dilution’, whereby native
hosts experience lower parasite burdens in the presence of
introduced hosts (Telfer et al. 2005; Kelly et al. 2009a;
Thieltges et al. 2009). While reduced parasite burdens in
native hosts may appear of less concern, alterations to processes that regulate population densities may have flow-on
effects on native species dynamics, such as the modification
of competitive advantage between conspecifics (Kopp &
Jokela 2007), which could result in subsequent alterations to
2011 The Authors. Journal of Animal Ecology 2011 British Ecological Society
Trout alter native host–parasite dynamics 991
community dynamics and ecosystem functioning. The frequency with which introduced species acquire native parasites and attain high population densities means there is
much potential for either parasite spillback or dilution to
occur.
Our current understanding of the potential impacts of
introduced species on native host–parasite interactions
relies largely on field-based observations of introduced
populations, using a combination of parasite fitness
parameters at individual (e.g. size, fecundity) and population scales (e.g. prevalence, infection intensity, abundance;
Bush et al. 1997) to assess the competency of introduced
species as native parasite hosts (Rauque, Viozzi & Semenas 2003). Such assessments have been made with or
without sympatric native host populations (Galli et al.
2005), and occasionally native parasite dynamics have
been surveyed within native-only host populations to provide baselines from which the effects of an introduced
host are judged (Dubois, Marcogliese & Magnan 1996;
Kelly et al. 2009a). However, native populations free
from the effects of introduced species are not always
available for such comparisons to be made.
While field-based observations are essential to ascertain
which native parasites have been acquired by introduced species and to identify patterns, differences in parasite fitness
parameters between native and introduced hosts may not
provide a true reflection of a parasite’s overall performance.
Field observations can obscure differences in establishment
success, survival ⁄ mortality, maturation, growth and relative
fecundity. For example, poor host competency of an introduced host in terms of parasite establishment could be
masked if this species was more likely to encounter infectious
stages, resulting in similar levels of prevalence and ⁄ or infection intensity in native and introduced populations. Similarly, comparable numbers of mature parasites in native and
introduced hosts might suggest equal compatibility for a
native parasite in both hosts, but field observations of parasite maturity cannot take into account differing maturity
rates between native and introduced hosts.
Recognizing the potential limitations of field observations,
some researchers have used experimental infection trials to
allow differences in parasite fitness between hosts to be verified under standard conditions (King, van Oosterhout &
Cable 2009; Thieltges et al. 2009). However, even this
approach fails to account for the dynamics of the whole
host–parasite system in terms of relative abundances of host
populations, infection encounter rates by intermediate hosts
and potential host behavioural changes caused by the presence of an introduced species. For example, hosts that occur
at high densities are more likely to influence parasite dynamics than less common hosts.
Here, we provide an in-depth assessment of parasite fitness
in native and introduced hosts in a system previously identified
as one in which the acquisition of native parasites by an
introduced species results in the dilution of parasites in native
hosts (Kelly et al. 2009a). We utilize a multiple-scale approach
of field observations, experimental trials and dynamic popula-
tion modelling to examine this complex system and identify
mechanisms responsible for observed field patterns.
Materials and methods
STUDY SYSTEM
In New Zealand, the introduced brown trout (Salmo trutta L.) is
a dominant freshwater fish considered responsible for the decline
and local extinction of native fish species (Townsend 2003). Since
its introduction as parasite-free eggs in 1867 (MacCrimmon &
Marshall 1968), more than 10 native parasite species have been
acquired by brown trout, including the generalist freshwater acanthocephalan Acanthocephalus galaxii Hine (Hine, Jones & Diggles
2000). In the Otago province of the South Island of New Zealand, this acanthocephalan has been reported from sympatric
stream populations of native roundhead galaxias (Galaxias anomalus Stokell) and brown trout (Kelly et al. 2009a). The parasite
matures in the intestine of the definitive fish host and releases eggs
into the water column via fish faeces. Larval cystacanth stages
develop in the intermediate amphipod host Paracalliope fluviatilis
Thomson after egg ingestion, with the life cycle of A. galaxii completed following predation of infected amphipods by the definitive
host (Hine 1977). Brown trout are a major predator of galaxiids
(Crowl, Townsend & McIntosh 1992; Townsend 1996) and thus
may acquire additional A. galaxii infections via postcyclic transmission when roundhead galaxias are eaten. This additional transmission route has been reported in many acanthocephalan species,
including native acanthocephalans transmitted from native galaxias to introduced trout in Argentina (Rauque, Semenas & Viozzi
2002), but has not been experimentally demonstrated for A. galaxii. Preliminary field observations suggest that A. galaxii attains
equal or higher prevalence and infection intensity in brown trout
(Kelly et al. 2009a), indicating the potential for modification of
parasite–host dynamics by this introduced host.
FIELD SURVEYS
Field surveys were conducted to determine the prevalence (the percentage of infected hosts) and infection intensity (the number of
worms per host; sensu Bush et al. 1997) of A. galaxii in its definitive
and intermediate host species, and the relative densities of these hosts
at three sites previously identified by Kelly et al. (2009a) as ‘sympatric’ for roundhead galaxias and brown trout infected with A. galaxii:
Swin Burn Q1 (2296¢90¢¢E, 5558¢70¢¢N), Swin Burn Q2
(2298¢30¢¢E, 5559¢40¢¢N) and Old Hut Creek (2294¢00¢¢E,
5568¢73¢¢N), all in the upper Taieri River catchment in Otago. Each
site was visited on 4–5 occasions between June 2007 and August 2008
to monitor temporal changes in host and parasite populations. Fish
densities at each site were assessed by single-pass electric fishing of
the same reach (230–416 m2) on each occasion. Random subsamples
of roundhead galaxias (n = 5–27) and brown trout (n = 1–16) from
each site were euthanized, measured for fork length (FL) to the nearest 1 mm and preserved in 10% buffered formalin. In the laboratory,
the alimentary canal from oesophagus to anus of each fish was
removed and split longitudinally. The abundance of acanthocephalans was noted, and the length (lm) and sex of each worm were
recorded. In addition, for female worms, developmental status (F1 –
immature with ovarian balls only, F2 – maturing eggs, F3 – fully
mature eggs) and proportion of mature eggs in a subsample of 50
eggs were also recorded. The number of P. fluviatilis and prey fish
2011 The Authors. Journal of Animal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 990–998
992 R. A. Paterson et al.
present in fish stomachs was also enumerated, to assess the relative
importance of cystacanth and postcyclic infection pathways.
The prevalence of infection in the intermediate amphipod host
P. fluviatilis was measured on each site visit from a 3–5-min kick
sample spread diagonally across the stream to sample all microhabitats. Amphipods were preserved in 10% formalin and up to 1000
amphipods from each sample were examined for the presence of
cystacanths.
INFECTION EXPERIMENT
An infection experiment was conducted to determine the fitness
of A. galaxii worms in both definitive hosts, from which relative
rates of parasite establishment, maturation and mortality could
be estimated. Brown trout (131–191 mm) and roundhead galaxias
(60–75 mm) were collected by electric fishing from the Cap Burn
(2295¢56¢¢E, 5546¢22¢¢N) and a tributary of the Kye Burn
(2293¢23¢¢E, 5563¢67¢¢N), and acclimatized in the University of
Otago’s controlled climate facilities (13-h day ⁄ 11-h night period,
10C, 15% daily water change, fed ad libitum with commercial
pellets) for 6 months prior to experimentation. All experimental
fish were treated with the anthelmintic Tetramisole HCl
(10 mg L)1 48 h · 2 repeat) at the beginning of the acclimatization period to remove any naturally acquired parasites prior to
artificial infection. Infection status prior to the experiment was
investigated by autopsy of five-treated and five-untreated fish per
species, during which no intestinal parasites were found in treated or untreated fish. Six experimental fish of each species were
randomly assigned to two infection time-periods (2 or 6 weeks).
During the 48 h prior to experimental infection, each fish was
measured (FL) and placed without food into an individual tank
(tank size: 15 L – roundhead galaxias, 30 L – brown trout).
Intermediate infective stages of A. galaxii were obtained by collecting naturally infected P. fluviatilis amphipods by handnet from
the Swin Burn (2298¢30¢¢E, 5559¢40¢¢N). Infection status was determined under a dissection microscope. A subsample of 15 amphipods
identified as infected was autopsied to assess observer error in correctly identifying the presence of A. galaxii, with single infections of
A. galaxii correctly identified in all amphipods. Ten live infected
A. galaxii amphipods were placed into each tank. The number of amphipods consumed by each fish was monitored by checking for uneaten individuals 24- and 48-h postexposure. All unconsumed
amphipods were removed at 48-h postexposure, and fish resumed
their diet of ad libitum commercial fish pellets. At the completion of
each infection period (2 or 6 weeks), fish were euthanized and immediately examined for parasites prior to fixing all acanthocephalans in
10% buffered formalin. Worm measurements were made as in the
field survey.
STATISTICAL ANALYSES
Statistical analyses of field survey and experimental infection data
were conducted using spss Statistic 15.0 (SPSS 2006). Parametric tests
were used for all analyses, for which data were transformed when
necessary to meet the normality assumptions of analysis of variance
(anova).
POPULATION MODEL
A population model was constructed using model maker 4.0 (Cherwell
2000) to dynamically simulate the influence of brown trout presence
on A. galaxii in its definitive hosts.
Model formulation
The life cycle of A. galaxii was modelled using a series of linked differential equations that simulate (on a daily basis, scaled to 1 m2) the
populations of uninfected (ANP) and infected (AP) amphipods, the
populations of immature and mature A. galaxii worms in roundhead
galaxias (IG, WG) and trout (IT, WT), and the number of A. galaxii
eggs in the environment (E), in discrete time steps:
dANP
¼ ðkA S þ rexðANP þAP Þ 1 CT T CG G vEÞANP
dt
eqn 1a
dAP
¼ vEANP þ ðrexðANP þAP Þ 1ÞX þ ðCT T þ CG GÞY AP
dt
eqn 1b
dIG
¼ CG GYc AP ðmG þ aG þ bG þ DTÞIG
dt
eqn 2a
dIT
¼ cTðCT YAP þ DIG Þ ðmT þ aT þ bT ÞIT
dt
eqn 2b
dWG
¼ mG IG ðaG þ bG þ DTÞWG
dt
eqn 3a
dWT
¼ mT IT þ cDTWG ðaT þ bT ÞWT
dt
eqn 3b
dE
¼ ðWG þ WT ÞkW ðe þ vANP ÞE
dt
eqn 4
The amphipod population was dynamically modelled to reflect
changing amphipod densities throughout the year while fish densities
were held constant (T and G for trout and galaxias, respectively)
because field surveys indicate the latter remain relatively constant
throughout the year, and there is no evidence of parasite impact on
fitness (Kelly et al. 2009a).
The population of uninfected amphipods ANP (eqn 1a) increases as
a function of amphipod fecundity (kA) (toggled by S, a logic switch
denoting the breeding season) and decreases as a function of natural
mortality (r ) 1, where r is survival) influenced by density dependence (x), predation by trout (CT) and galaxias (CG), and infection
(m).
The population of infected amphipods AP (eqn 1b) increases as a
function of infection (v), and is modified by a combination of natural
mortality (r ) 1) modified by density dependence (x) and infection
(X), and the predation of infected amphipods by trout (CT) and galaxias (CG), also modified by infection (Y). The parameter Y acknowledges that the presence of the parasite can be expected to increase the
likelihood that an amphipod will be eaten. If the rate at which uninfected amphipods ingest acanthocephalan eggs exceeds the number
of uninfected amphipods, all amphipods are considered to be
infected.
The population of immature worms in galaxias IG (eqn 2a)
increases with the predation of infected amphipods (CGY), modified
by establishment success (c). The number of immature worms
decreases with worm maturation (mG), parasite mortality (aG),
2011 The Authors. Journal of Animal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 990–998
Trout alter native host–parasite dynamics 993
natural host mortality (bG) and postcyclic transmission of worms
from galaxias to trout (D). The population of immature worms in
trout IT (eqn 2b) increases with the predation of infected amphipods
(CTY) and postcyclic transmission (D), both modified by establishment success (c), and decreases with worm maturation (mT), worm
mortality (aT) and natural host mortality (bT).
The population of mature worms in galaxias WG (eqn 3a) increases
as a function of worm maturation (mG) and decreases with parasite
mortality (aG), natural host mortality (bG) and postcyclic transmission (D). The population of mature worms in trout WT (eqn 3b)
increases as a function of worm maturation (mT), the establishment
(c) of postcyclically transmitted worms from galaxias to trout (D),
and decreases because of the effects of parasite mortality (aT) and
natural host mortality (bT). A density dependence parameter influencing worm survival was not incorporated into immature or mature
worm equations, as very low field infection intensities of A. galaxii
were observed in the species modelled in contrast to burdens recorded
from other galaxias hosts in New Zealand (cf. Galaxias maculatus
mean infection intensity 127 per fish; Hine 1977).
The number of A. galaxii eggs in the environment E (eqn 4)
increases as a function of the number of eggs produced (kW) from
mature worms in both galaxias (WG) and trout (WT), and decreases
with natural mortality (e) and the ingestion of eggs by amphipods (v).
Model parameterization
Parameter estimates were obtained, where possible, from the field
surveys and experimental infections reported here, and from the published literature and unpublished data (see Tables 1 and 2). Host densities (G, T) were calculated as the average number of fish per m2 at
Swin Burn Q1 and Q2 combined (Old Hut Creek was not included in
the parameterization of the model as only a single A. galaxii infection
was recorded there). The daily mortality rate of brown trout was
based on a maximum life span of 5–6 years for nonmigratory brown
trout (Huryn 1996), whereas the mortality rate of roundhead galaxias
was estimated from a closely related species, Galaxias paucispondylus
(Bonnett 1990).
Mean amphipod density was estimated as 250 amphipods per m2
(Weller 2003), with natural survival estimated from the maximum life
span of 1 year (F. Wilhelm, unpublished). The daily fecundity rate of
0Æ058 new individuals per amphipod during the breeding season (September to March, austral spring to end of austral summer) was estimated from a maximum of 3Æ5 broods of five eggs per female and a
0Æ5 sex ratio (F. Wilhelm, unpublished). However, as a proportion of
females are known to breed year round (Towns 1981), breeding from
April to August (austral autumn and winter) was set at 20% of the
maximum.
The probability of amphipods being consumed by each definitive
host was calculated as the average number of amphipods in the host
gut (with an assumed gut clearance time of 48 h; Tekinay, Guner &
Davies 2003) relative to amphipod density (field survey). The potential for postcyclic transmission of parasites from galaxias to trout
was calculated from the average number of roundhead galaxias present in the stomachs of brown trout in the field surveys.
Although acanthocephalans have been shown to markedly alter
intermediate host behaviour (Baldauf et al. 2007), often increasing
the likelihood that infected individuals will be eaten (Moore 1984;
Lagrue et al. 2007), no information is available about how A. galaxii
alters the risk of being eaten (Y) or mortality (X) of its amphipod
host. Likewise, no information is available about amphipod density
dependence (x) or parasite egg ingestion rate by amphipods (m).
These parameters were estimated by model optimization to the values
Table 1. Definitive host parameter definitions and estimates used in the population model
Galaxias
Trout
Parameter
Symbol
Value
Symbol
Value
Units
Source
Density
Predation of amphipods
G
CG
0Æ0763
0Æ00047
T
CT
0Æ0117
2e)05
This study
This study
Parasite establishment
Parasite mortality
Parasite maturation
Natural host mortality
c
aG
mG
bG
0Æ5078
0Æ01869
0Æ006
0Æ0007
c
aT
mT
bT
0Æ5078
0Æ0416
0Æ000
0Æ0004
m)2
amphipod per host
per day
per worm
per worm per day
per worm per day
per host per day
Predation of galaxias
–
–
D
0Æ01
per galaxias per trout
per day
This study
This study
This study
Bonnett (1990),
Huryn (1996)
This study
Table 2. Intermediate host and parasite parameter definitions and estimates used in the population model
Parameter
Symbol
Value
Units
Source
Amphipod breeding rate
Amphipod natural mortality
Parasite fecundity
Ingestion rate of eggs by amphipods
Egg mortality
Amphipod density dependence
Parasite influence on amphipod mortality
Parasite influence on amphipod predation
kA
r
kW
M
E
x
X
Y
0Æ058
0Æ0027
807Æ5
6e)06
0Æ005
0Æ0001
26Æ68
40Æ36
per amphipod per day
per amphipod per day
per worm per day
per egg per amphipod per day
per egg per day
per amphipod per day
per amphipod per day
per amphipod per day
F. Wilhelm, unpublished data
F. Wilhelm, unpublished data
Crompton & Whitfield (1968)
This study
Crompton (1970)
Model optimization
Model optimization
Model optimization
2011 The Authors. Journal of Animal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 990–998
994 R. A. Paterson et al.
that result in predicted levels of prevalence and infection intensity, in
both intermediate and definitive hosts, equivalent to those observed
in the field (a mean population size of 250 m)2 for uninfected amphipods, a mean prevalence of infected amphipods of 0Æ1%, and a mean
worm population size of 0Æ1 m)2 at equilibrium dynamics). Once an
amphipod becomes infected with a single A. galaxii, we assumed it
does not consume additional eggs. This assumption does not affect
model dynamics as eggs are highly abundant in the environment, and
prevalence of amphipod infection is low.
The establishment, maturation and mortality rates of A. galaxii in
each definitive host were estimated from the infection experiment.
Parasite establishment at day one and the daily mortality rate of
A. galaxii in galaxias were estimated from the slope of the line calculated from the percentage of worms present at 2 and 6 weeks postinfection. No worms were present in trout at 6 weeks postinfection, so
parasite establishment rate in trout was assumed to be the same as in
galaxias, while parasite mortality rate was estimated from the decline
to zero parasites at 6 weeks. No mature worms were present in trout
from either the experimental infection or field survey; thus, the maturity rate in trout was set at 0.
The daily rate of parasite egg production was estimated from the
acanthocephalan, Polymorphus minutus (1700 eggs per female per
day; (Crompton & Whitfield 1968), divided by the overall parasite
male:female ratio observed in the current study. Egg mortality was
based on aquatic acanthocephalan eggs being known to survive a
maximum of 6–9 months (Crompton 1970).
Model simulation
Although brown trout are known to have altered freshwater fish
communities in New Zealand, resulting in the declining abundance
and localized extinction of some Galaxias species (Townsend 2003),
their influence on native host–parasite dynamics is largely unknown.
Here, we use model simulations to examine the influence of brown
trout on native parasite dynamics in roundhead galaxias by investigating varying ratios of fish community composition that represent
(i) fish communities prior to trout introduction (galaxias scenario),
(ii) trout presence in native communities (galaxias + trout scenario)
and (iii) localized extinction of native fish (trout scenario). To understand how the presence of the exotic host might be influencing
observed levels of infection in the native host, we use sensitivity analyses to test the validity of potential contrasting hypotheses in the
galaxias + trout scenario: (i) brown trout out-compete roundhead
galaxias for infected amphipods (varying CT), (ii) brown trout prey
on roundhead galaxias (varying D) and (iii) brown trout modify the
behaviour of roundhead galaxias, resulting in altered consumption
of infected amphipods (varying CG).
Simulations were run varying the above parameters ± 100%
around their estimated value in 10% increments, to investigate the
influence of each parameter on the infection intensity of A. galaxii in
roundhead galaxias. For each scenario, we monitored peak density
of A. galaxii in the roundhead galaxias population (m)2) after 3000
daily iterations.
Results
FIELD SURVEY
Roundhead galaxias was the most abundant definitive host
in surveyed streams, with average densities of 0Æ05–0Æ20 fish
per m2 for roundhead galaxias and 0Æ005–0Æ07 fish per m2 for
brown trout. A total of 219 of 537 roundhead galaxias (39–
91 mm) and 84 of 126 brown trout (63–189 mm) were examined for A. galaxii. At Old Hut Creek, 72 galaxias and 34
trout were examined, but only a single A. galaxii infection
was recovered from one roundhead galaxias on a single occasion (in June 2007). This site was removed from further analysis of field survey observations.
Infection prevalence did not differ significantly between
sites or host species (GLM; P > 0Æ05), with the percentage
of fish infected ranging from 12Æ5% to 85% for roundhead
galaxias and 0–100% for brown trout (Table 3). Infection
intensities were highest in brown trout (natural log transformed: GLM species; F1,93 = 4Æ977, P = 0Æ028) but did not
Table 3. Seasonal prevalence, infection intensity and length Acanthocephalus galaxii in naturally infected roundhead galaxias and brown trout
from sites Q1 and Q2 on the Swin Burn
Site
Q1
Host
Species
Roundhead
galaxias
Brown trout
Q2
Roundhead
galaxias
Brown trout
Season
No.
of
hosts
Jun 07
Oct 07
Mar 08
May 08
Aug 08
Jun 07
Oct 07
Mar 08
May 08
Aug 08
Oct 07
Mar 08
May 08
Aug 08
Oct 07
Mar 08
May 08
Aug 08
10
27
16
20
19
0
6
3
1
0
20
10
20
5
14
4
2
2
Prevalence %
Infection
intensity
(mean ± SD)
Male length
lm (mean ±
SD)
Female length
lm (mean ±
SD)
No.
of
parasites
40
40Æ7
12Æ5
45
52Æ6
–
83Æ3
100
0
–
80
80
85
60
85Æ7
75
50
100
2Æ8 ±
6Æ6 ±
5
16Æ6 ±
11Æ2 ±
–
12Æ6 ±
13Æ7 ±
–
–
11Æ2 ±
1Æ5 ±
4Æ1 ±
5Æ7 ±
10Æ8 ±
6Æ3 ±
27
10
1725 ±
2376 ±
2600 ±
1699 ±
2057 ±
–
1210 ±
1039 ±
–
–
1851 ±
2346 ±
2108 ±
1642 ±
943 ±
1378 ±
1254 ±
1478 ±
4800 ±
3002 ±
4350 ±
2447 ±
3403 ±
–
1141 ±
1162 ±
–
–
2520 ±
2720 ±
3349 ±
3255 ±
967 ±
1295 ±
1405 ±
1475 ±
11
72
10
149
112
–
63
41
–
–
179
12
65
17
129
19
27
20
1Æ5
6Æ3
19Æ7
16
14Æ6
16Æ8
22Æ4
0Æ5
3Æ8
4Æ7
12Æ1
3Æ8
527
1023
650
563
393
323
239
713
940
716
391
193
370
192
311
566
1844
1222
963
1221
266
232
1374
952
1665
900
180
341
208
293
2011 The Authors. Journal of Animal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 990–998
Trout alter native host–parasite dynamics 995
Q1
Q2
Worms in galaxias
100%
80%
60%
40%
20%
0%
80%
60%
40%
20%
0%
Jun 07
Oct 07
differ between sites or seasons. Acanthocephalans were larger
in roundhead galaxias than brown trout (GLM species;
F1,220 = 24Æ803, P < 0Æ001), with female worms larger than
male worms (GLM sex; F1,220 = 5Æ965, P = 0Æ015). All
female worms recovered from brown trout were immature
with ovarian balls present only, while on average 18Æ6% of
female worms in roundhead galaxias contained developing
eggs (F2) or fully mature shelled eggs (F3) (Fig. 1).
Examination of stomach contents showed that 71% of
brown trout stomachs contained amphipods, with an average
of 14Æ9 amphipods per fish, while 17% of roundhead galaxias
stomachs contained amphipods, with an average of two amphipods per fish. Fourteen per cent of brown trout stomachs
also contained roundhead galaxias, with between one and
three galaxias present. Prevalence of infection in amphipods
collected from kick samples was very low at all sites, with a
maximum of 0Æ1% of amphipods infected.
INFECTION EXPERIMENT
Similar percentages of worms had established in each host
species at 2 weeks postinfection, with an average of 38Æ6% of
worms establishing in roundhead galaxias and 28Æ0% in
brown trout (one-way anova species; P = 0Æ465; Fig. 2). The
intensity of infection declined in both species between 2 and
6 weeks postinfection, with 19Æ2% of worms remaining in
galaxias and no worms in trout (Fig. 2).
Male A. galaxii were larger in brown trout than in roundhead galaxias at 2 weeks postinfection (one-way anova male;
F1,14 = 5Æ948, P = 0Æ030), while female worms were of similar length (P = 0Æ136, Table 4). Worm size increased
between 2 and 6 weeks postinfection, with average male and
female lengths in galaxias at 6 weeks postinfection greater
than in trout at 2 weeks postinfection. No gravid female
Mar 08 May 08 Aug 08
Jun 07
Oct 07
Time
Mar 08
May 08
Aug 08
Time
Male
Non-gravid female
Gravid female
60
Trout
Establishment %
Fig. 1. Seasonal composition of Acanthocephalus galaxii sex and reproductive status
in roundhead galaxias and brown trout at
sites Q1 and Q2 on the Swin Burn. Gravid
female worms with maturing eggs (F2) or
fully mature shelled eggs (F3) were absent
from brown trout throughout the study
period.
Worms in trout
100%
Galaxias
40
20
0
2
6
Week
Fig. 2. Establishment (2 weeks) and survival (6 weeks) of Acanthocephalus galaxii in experimentally infected roundhead galaxias and
brown trout. Establishment success did not differ between hosts
(P > 0Æ05).
worms were present in either host species at 2 weeks postinfection, while one of four female worms present in galaxias at
6 weeks postinfection was gravid.
POPULATION MODEL
Model simulations of varying fish community composition
indicated that a minimum proportion of 70% galaxias in the
total fish community is the threshold for the survival of
A. galaxii, below which the native parasite rapidly goes
extinct (Fig. 3). At the current field densities of the total fish
community (0Æ088 individuals per m2), densities of A. galaxii
infection in galaxias are predicted to be only slightly lower
than would be expected if trout were absent from the system,
as the ability of trout to act as an infection sink is weakened
by the low relative density of this introduced host.
Changing the rate of predation by brown trout on either
amphipods or roundhead galaxias had little influence on the
2011 The Authors. Journal of Animal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 990–998
996 R. A. Paterson et al.
Table 4. Prevalence, infection intensity, length and reproductive status Acanthocephalus galaxii in experimentally infected roundhead galaxias
and brown trout. Gravid females represent females with maturing eggs (F2) and fully mature shelled eggs (F3)
Host
Week
No. of
hosts
Prevalence %
Infection intensity
(mean ± SD)
Roundhead
galaxias
2
6
100
3Æ3 ± 2Æ5
6
6
50
2Æ3 ± 1Æ5
2
6
100
2Æ6 ± 1Æ9
6
6
0
0
Length lm
(mean ± SD)
No. of
parasites
M
F1
M:F ratio
M
F1
F2
M:F ratio
M
F1
M:F ratio
–
1806
2097
1:1Æ6
2191
2783
2425
1:1Æ3
2128
2338
1:1Æ3
–
± 84
± 108
8
12
0
± 141
± 65
3
3
1
25
± 103
± 103
7
9
0
–
–
Gravid
females %
(a)
0·4
0·2
0·3
0·2
0·1
0·1
0·0
0
0
20
40
60
80
100
% Galaxias
Fig. 3. Density of Acanthocephalus galaxii infections in roundhead
galaxias (filled circle) and brown trout (open circle) in relation to percentage of galaxias in the combined total fish population (0Æ088 fish
per m2) predicted from model simulations. The dashed line represents
the current percentage of galaxias in the total fish population as
recorded in the field survey.
Acanthocephalus galaxii density m–2
Acanthocephalus galaxii density m–2
Brown trout
Parasite sex
(b)
0·4
0·3
0·2
0·1
0·0
(c)
0·4
density of A. galaxii in the modelled roundhead galaxias
population (Fig. 4a,c). In contrast, A. galaxii densities in
roundhead galaxias were highly sensitive to changes in the
rate of predation on amphipods by this fish (Fig. 4b), with
predation rates below 0Æ004 per amphipod per host per day
()20%) resulting in extinction of the parasite.
0·3
0·2
0·1
0·0
–100
–50
0
50
100
% Change
Discussion
We used a combination of field observations, experimental
infections and dynamic population modelling to examine the
influence of an introduced species on a native host–parasite
system. Our field observations indicated that although the
prevalence and infection intensity of A. galaxii were similar
in introduced trout and native galaxias, the native parasite
attained smaller sizes and failed to mature in the introduced
host. Our experimental infection results showed trout to be
similar to galaxias in its competence as a host in terms of parasite establishment and initial growth, but trout was found to
be unsuitable for maintaining A. galaxii populations, as
Fig. 4. Simulating the effect on the density of Acanthocephalus galaxii infections in roundhead galaxias of altering (a) trout predation on
amphipods CT, (b) galaxias predation on amphipods CG and (c) trout
predation on galaxias (D). Each estimate was modified ± 100% of
current estimates in 10% increments.
worms did not reach maturity. Hence, the field and experimental results suggested that trout were likely to act as an
infection sink because of poor host competency. However,
the population model indicated that the influence of this
mechanism on the dynamics of A. galaxii in its native host
2011 The Authors. Journal of Animal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 990–998
Trout alter native host–parasite dynamics 997
would be limited because of only a small proportion of the
total fish community being comprised of trout. In contrast,
our model suggested that trout presence may have more substantial consequences for the native parasite population by
altering amphipod consumption by roundhead galaxias, with
such consequences being greater at higher trout densities.
FIELD OBSERVATIONS
Field observations are often the first source of information
used to determine the influence of introduced species on
host ⁄ parasite dynamics. For example, Telfer et al. (2005)
used field surveys to determine the influence of the introduced
bank vole (Myodes glareolus) on Bartonella sp. infections in
native wood mice (Apodemus sylvaticus), concluding that
infection prevalence in wood mice decreased with increasing
bank vole density. Moreover, Rauque, Viozzi & Semenas
(2003) used the results of field surveys to demonstrate that
parasites in the introduced rainbow trout (Oncorhynchus mykiss) contributed 20% of total egg output by the native acanthocephalan parasite Acanthocephalus tumescens. Field
observations may provide useful insights into the potential
impacts of introduced species on native parasite–host
dynamics. However, as demonstrated by our study, assessment of parasite maturation is needed in addition to observations of infection prevalence and intensity to determine the
impact of an introduced species.
INFECTION EXPERIMENT
Our experimental infections generally supported the fieldbased conclusions that trout are inferior hosts of A. galaxii,
yet interestingly A. galaxii initially experienced similar establishment success and equivalent or greater growth in this
host. Although worms in galaxias were relatively slower
growing, in the long term they attained larger sizes than in
trout. Most importantly, A. galaxii worms failed to reach
maturity in brown trout; thus, the introduced host was
unsuccessful at supporting this stage of the parasite’s life
cycle.
POPULATION MODEL
The population model revealed that the density of A. galaxii
in roundhead galaxias may only be slightly reduced as a result
of parasite dilution by trout. In sensitivity analyses, modifying either the rate at which trout feed on roundhead galaxias
or on amphipods caused little change to the native parasite’s
density in its native roundhead galaxias host. However,
decreasing the rate of amphipod predation by roundhead galaxias markedly decreased the parasite’s adult population.
The model also revealed that parasite burdens were highly
sensitive to relative host abundances. Hence, a correlation
between increasing trout presence and decreasing native parasitism of roundhead galaxias, as observed for the parasite
Deretrema philippae by Kelly et al. (2009a), may just as likely
be caused by trout reducing galaxias density or altering their
foraging behaviour, rather than trout serving as an infection
sink. This conclusion is supported both by demonstrations
that trout predate galaxias (Crowl, Townsend & McIntosh
1992; Townsend 2003) and experimental studies of habitat
use by native galaxiids in the presence of brown trout (McIntosh, Townsend & Crowl 1992), which showed that trout
out-compete Galaxias spp. in streams, forcing them to forage
in areas with lower invertebrate drift.
Native parasite loss through dilution or via other mechanisms, such as altered predation on intermediate hosts by
native species, is a largely unrecognized consequence of the
invasion of introduced species. Most commonly, invasion
biology research has focused on the impacts of introduced
species on native conspecifics via predation and ⁄ or competition and through the introduction of novel parasites. However, as native parasites play major roles in the structuring of
native communities, neglecting the potential for native parasite loss subsequent to the arrival of exotic species overlooks
a potentially important consequence of invasions.
LIMITATIONS AND STRENGTHS OF DYNAMIC
POPULATION MODELS
We acknowledge that the strength of population simulation
models in depicting ‘real-world’ dynamics is only as good as
the data used to parameterize them. In the present study, we
utilized field information from multiple sites and seasons,
experimental infections and published literature to generate
the majority of parameter estimates. However, we were
unable to draw on these sources to estimate the amphipod’s
mortality and predation risk, although the dynamic model
suggested that A. galaxii infections are strongly influenced
by both parameters. Manipulation of intermediate host
behaviour to enhance transmission success via predation is a
common strategy of parasites that utilize hosts at different
trophic levels and is frequently adopted by acanthocephalans
(Moore 1984; Poulin 1995). Acanthocephalan infections in
amphipods have also been reported to alter host immune
responses to bacterial infections, potentially increasing intermediate host mortality (Cornet et al. 2009). Experimental
studies are required to fully quantify the mechanism and
degree to which A. galaxii infection alters the mortality and
predation risk of amphipods, and to identify whether
behavioural responses of infected amphipods to predator
presence differ between native and exotic fish.
Acknowledgements
We thank D. Kelly, M. Green and A. Lal for field and laboratory assistance,
and F. Wilhelm for P. fluviatilis life-history information. We are also grateful
to R. Scott and D. Crutchley for site access. Permission was obtained from the
Department of Conservation, NZ Fish and Game and the University of Otago
Animal Ethics Committee (ET 16 ⁄ 7). Funding for this research was provided
by the Royal Society of New Zealand Marsden Fund.
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Received 31 May 2010; accepted 22 February 2011
Handling Editor: Mike Boots
2011 The Authors. Journal of Animal Ecology 2011 British Ecological Society, Journal of Animal Ecology, 80, 990–998