Environ Biol Fish (2008) 83:99–105
DOI 10.1007/s10641-007-9228-3
S P E C I A L I S S U E C H A RR
Gyrodactylus salaris (Monogenea, Gyrodactylidae)
infections on resident Arctic charr (Salvelinus alpinus)
in southern Norway
Grethe Robertsen Æ Kjetil Olstad Æ
Laetitia Plaisance Æ Lutz Bachmann Æ
Tor A. Bakke
Received: 15 October 2006 / Accepted: 16 January 2007 / Published online: 14 February 2007
Springer Science+Business Media B.V. 2007
Abstract This study surveys the distribution of
Gyrodactylus salaris on resident Arctic charr,
Salvelinus alpinus, in lakes connected to three
south-Norwegian watercourses: Numedalsvassdraget, Skiensvassdraget and Hallingdalsvassdraget. Gyrodactylus salaris infected charr was only
recorded in Numedalsvassdraget. The parasites
had the same mitochondrial haplotype as those
previously reported on charr in Lake Pålsbufjorden, which is part of Numedalsvassdraget. Since
the G. salaris-charr association is persistent in
Pålsbufjorden and has a wide distribution above
the stretches of the watercourse inhabited by
anadromous salmonids, this is considered a stable,
although perhaps relatively young, host-parasite
system. More detailed analyses of these interactions revealed seasonal variations in the parasite
population dynamics between late summer and
late autumn, with heavier infections occurring in
males and older fish in October. This is explained
G. Robertsen (&) K. Olstad L. Plaisance L. Bachmann T. A. Bakke
Department of Zoology, Natural History Museum,
University of Oslo, P.O. Box 1172, Oslo NO-0318,
Norway
e-mail: grethe.robertsen@nhm.uio.no
Present Address:
L. Plaisance
Scripps Institution of Oceanography, University of
California, San Diego, 8750 Biological Grade, Hubbs
Hall, La Jolla, CA 92037, USA
by the combined action of seasonal differences in
temperature and physiology and ecology of host
cohorts. It is assumed that the occurrence of G.
salaris on charr in Pålsbufjorden resulted from a
host switch to charr from rainbow trout, Onchorynchus mykiss. Host switches may cause significant expansions of the geographical range of
pathogenic variants of G. salaris. Therefore, observations of frequently occurring G. salaris on charr
have implications for the diagnosis, management
and control of salmonid gyrodactylosis.
Keywords
Distribution Epidemiology
Introduction
Monogeneans of the fish ectoparasitic genus
Gyrodactylus von Nordmann, 1832 encompasses
species with both narrow and broad host specificity (Bakke et al. 2002). Of the >400 valid Gyrodactylus species known, nine have been recovered
from species of the genus Salvelinus (see Harris
et al. 2004). Arctic charr, Salvelinus alpinus, is the
only species of the genus Salvelinus with a
circumpolar distribution and a natural distribution
in Norway. Freshwater resident Arctic charr
populations are occurring all over Norway,
whereas anadromous populations are restricted
to northern Norway (Klemetsen et al. 2003).
Gyrodactylus salaris, that has Atlantic salmon,
123
100
Salmo salar L., as type host, has so far been found
on resident charr in Lake Pålsbufjorden in southern Norway and on anadromous charr in two
north Norwegian localities (Mo 1988; Knudsen
et al. 2006; Robertsen et al. 2007). The G. salaris
infected resident charr do not co-occur with
Atlantic salmon whereas the anadromous charr
is sympatric with infected Atlantic salmon.
Gyrodactylus salaris is a severe pathogen of
Norwegian Atlantic salmon (see Johnsen et al.
1999), and experimentally it can infect and
reproduce (although not to a pathogenic level)
on other salmonids including anadromous and
resident Arctic charr (Bakke et al. 1996, 2002;
Olstad et al. 2007). While the G. salaris strain
infecting anadromous Arctic charr in the north
Norwegian localities is pathogenic to Atlantic
salmon, the strain on resident Arctic charr in
Pålsbufjorden is non-pathogenic to Atlantic
salmon in experiments (Olstad et al. 2007).
Fish parasite infections may be affected by
several macro- and microenvironmental factors.
Seasonality of several Gyrodactylus species
including G. salaris on salmon is well documented
(e.g. Chubb 1977; Johnsen and Jensen 1992;
Appleby and Mo 1997; Aydogdu 2006), and has
been reported for G. salaris infecting anadromous
charr in northern Norway (Kanck et al. 2006).
Host size and age are also well known to influence
the infection of freshwater monogeneans (Chubb
1977). Furthermore, the sex of the host may be
important for the population dynamics of G.
salaris. Male fish have been reported infected
with ectoparasites to a higher extent than females,
in particular sexually mature males during spawning time (Pickering and Christie 1980; Appleby
1996; Skarstein et al. 2001).
The aim of this study is to survey the distribution of G. salaris infections on resident Arctic
charr in three south-Norwegian watercourses, in
addition to analyze the Arctic charr-G. salaris
association in Lake Pålsbufjorden.
Materials and methods
Arctic charr, Salvelinus alpinus, were sampled in
five lakes of the Numedalsvassdraget watercourse
(Skurdalsfjorden, Pålsbufjorden, Tunhovdfjorden,
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Environ Biol Fish (2008) 83:99–105
Norefjorden and Kravikfjorden; Skurdalsfjorden
and Tunhovdfjorden were also sampled in 2003),
two lakes of the Hallingdalsvassdraget watercourse (Ustevann and Rødungen) and in one lake
in the Skiensvassdraget watercourse (Tinnsjøen;
was also sampled in 2003) during the autumn of
2005 (see Table 1, Fig. 1). All charr were sampled
by use of gill nets.
The fish were killed by a blow to the head
and the fins or the entire fish were immediately
fixed in 96% ethanol. The individual fish from
Pålsbufjorden were kept separate to analyze the
host–parasite dynamics in this locality, while the
other localities were sampeled only to track the
geographical distribution of G. salaris on Arctic
charr. In the laboratory, fish and fins were
screened for ectoparasites using a stereo-microscope. The gyrodactylids recovered were
removed from the fish and transferred into
Eppendorf tubes containing 96% ethanol and
stored at –20C.
The molecular identification of G. salaris relied
on the sequencing of the internal transcribed
spacers (ITS) of the nuclear ribosomal gene
cluster and the mitochondrial cytochrome oxidase
1 (COI) gene (see Cunningham et al. 2001;
Matějusová et al. 2001; Hansen et al. 2003;
Zie˛tara and Lumme 2003). 1–3 parasites per
population were individually used for molecular
analyses. BLASTN (Altschul 1991) searches were
conducted in order to find matching entries in
GenBank.
The opisthaptors from at least 10 specimens
from each locality were digested according to a
slightly modified version of Harris et al. (1999),
and the opisthaptoral hard parts were digitalized
in a Leica DC 500 camera mounted on a Leica
DM 6000B stereo microscope for morphological
analyses.
The counting of G. salaris on charr from
Lake Pålsbufjorden was performed using a
stereo-microscope. Of a total of 158 charr
sampled in this lake, 60 were screened on both
body and fins and 98 only on the fins. As few
parasites were detected on the bodies, all
further analyses are restricted to parasites
infecting the fins.
In order to study the population dynamic of
G. salaris infections, charr caught in
Environ Biol Fish (2008) 83:99–105
Table 1 The Arctic charr
populations sampled and
screened for G. salaris
infections in south
Norwegian lakes and
watercourses
Watercourses
Lakes
Numedalslågen
Skurdalsfjorden
†
†
Pålsbufjorden
†
Tunhovdfjorden
†
†
Norefjorden
Kravikfjorden
Hallingdalsvassdraget
Ustevann
†
†
Rødungen
Skiensvassdraget
Tinnsjøen
†
101
Sampling date
(dd.mm.yy)
Number of Arctic
charr
G. salaris
infection
10–19.10.03
23–26.08.05
03–04.10.05
22–26.08.05
11–14.10.05
04–05.08.03
10–11.09.03
23–24.08.05
26–27.10.05
25–26.10.05
92
26
70
57
101
30
12
6
150
35
–
–
+
+
+
–
+
–
+
+
16–17.08.05
05–07.09.05
03–06.10.05
29–31.08.05
2
26
30
2
–
–
–
–
02–03.11.03
18–19.10.05
10
111
–
–
(1991), and sex and gonad condition was
determined by dissection of the body.
The standard parameters, prevalence (proportion of the population infected), abundance
(mean number of parasites of both infected
and uninfected fish), and mean intensity (mean
number of parasites of infected hosts) were
determined for the G. salaris infections on
Arctic charr (after Bush et al. 1997). Chi-square,
Kruskal–Wallis, and Mann–Whitney U tests
were employed to test for statistically significant
differences in prevalence, abundance and mean
intensity between groups. All tests were performed with the program PAST version 1.29
(Hammer et al. 2001).
Fig. 1 The localities (lakes) in southern Norway surveyed
for G. salaris infections on Arctic charr and their
respective watercourses. A1: Tinnsjøen (Skiensvassdraget
watercourse); B1: Skurdalsfjorden, B2: Pålsbufjorden,
B3: Tunhovdfjorden, B4: Norefjorden, B5: Kravikfjorden
(Numedalsvassdraget watercourse); C1: Ustevann,
C2: Rødungen (Hallingdalsvassdraget watercourse) (see
Table 1)
Pålsbufjorden in August and October 2005 was
analyzed in more detail. The age of the charr
was determined by means of the otholiths
according to Kristoffersen and Klemetsen
Results
Arctic charr was found infected with G. salaris
only in the lakes Skurdalsfjorden, Pålsbufjorden,
Tunhovdfjorden, Norefjorden and Kravikfjorden,
all belonging to the Numedalsvassdraget water
course. The lakes are located above the stretches
of the river Numedalslågen inhabited by Atlantic
salmon (see Table 1; Fig. 1). Gyrodactylus salaris
was identified in all lakes based on ITS
sequences
(GenBank
Accession
number
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102
Environ Biol Fish (2008) 83:99–105
DQ898302), and the COI was identical to the
mitochondrial haplotype (GenBank Accession
number DQ923578) earlier detected in G. salaris
on charr from Pålsbufjorden (see Robertsen
et al. 2007). In addition, the opisthaptoral hard
parts were morphologically indistinguishable
from those of G. salaris previously described
from charr in Pålsbufjorden (Robertsen et al.
2007).
The prevalence of G. salaris on charr in
Pålsbufjorden was significantly higher in October
2005 (34.7%, n = 101) than in August 2005 (1.8%,
n = 57) (Chi-square test, P << 0.01; Table 2) as
was the abundance (Mann–Whitney U test,
P = 0.001; see Table 2). However, the mean
intensity was significantly higher in August than
in October (22 versus 6.4) due to one heavily
infected fish in August (Table 2).
Sex, age and maturity status was determined
for 74 of the 101 charr caught at the spawning
grounds in October (the rest was not possible to
link to infection data). Only 7 out of 74 fish were
not in spawning condition. The non-spawning fish
where 2, 3 and 4 years old.
There were significant differences in prevalence
of infection related to age and gender of the host.
In the lowest age group (2–3 years, n = 41) the
infection was significantly less than in older age
groups (4 years, n = 30; 5 years, n = 16; 6–7 years,
n = 14) (Chi-square tests, P < 0.05; Table 2). No
significant difference in prevalence was observed
between the age groups 4, 5, and 6–7 years (Chisquare tests, P > 0.05). Abundance differed
significantly between the four age groups
(Kruskal-Wallis test, P = 0.01). Pair-wise tests
revealed that the differences were between the
age group 2–3 years and the age groups 5 and 6–
7 years, respectively (Mann–Whitney U tests,
P < 0.05; Table 2). No significant differences were
found between the age groups with regard to
mean intensities (Kruskal–Wallis test, P = 0.15)
(Table 2).
The prevalence of infection of G. salaris on
male charr (n = 43) was significantly higher than
on female charr (n = 31) (Chi-square test, P =
0.017; Table 2), as was the abundance of infection
(Mann–Whitney U test, P = 0.01; Table 2).
However, the mean intensity of parasites on
males and females (7.6 versus 3.8; Table 2) did
not differ significantly (Mann–Whitney U test,
P = 0.052).
Discussion
The extended survey for G. salaris infections on
resident Arctic charr in three watercourses in
southern Norway revealed that only Numedalsvassdraget was infected with G. salaris. The
widespread G. salaris infections throughout
Numedalsvassdraget watercourse upstream of
the stretches populated with salmon, indicate that
charr is a more common host for G. salaris in
Norway than previously expected (Mo 1988;
Knudsen et al. 2006; Robertsen et al. 2007).
This is in line with the findings of Olstad et al.
(2007), who concluded from laboratory experiments with G. salaris from charr in Pålsbufjorden
that Arctic charr and rainbow trout were moderately susceptible, whereas Atlantic salmon from
rivers Numedalslågen and Drammenselva were
innately resistant to only slightly susceptible.
Table 2 Details on the G. salaris infection on Arctic charr in Lake Pålsbufjorden (Buskerud County, south Norway) in
August and October 2005, and the relation of infection to sex and age of the host in October
Month
Number of fish
Number of infected fish
Number of G. salaris
Prevalence
Abundance
Mean intensity
Standard deviation
123
Sex (October)
Age groups (years) (October)
August
October
Male
Female
2–3
4
5
6–7
57
1
22
1.8
0.4
22
2.9
101
35
225
34.7
2.2
6.4
7.3
43
23
175
53.5
4.1
7.6
8.9
31
8
30
25.8
0.97
3.8
3.4
41
6
61
14.63
1.49
10.17
7.3
30
11
29
36.7
0.97
2.6
1.6
16
9
94
56.3
5.9
10.44
13
14
9
41
64.29
2.93
4.55
5.1
Environ Biol Fish (2008) 83:99–105
The present study revealed seasonal variation
of the G. salaris infection on Arctic charr in
Pålsbufjorden as both prevalence and abundance
were significantly higher in October (water temperature: 8C) than in August (water temperature: 16C). This is congruent with earlier
observations of G. salaris experiencing a second
peak in abundance on Atlantic salmon in late
autumn (Mo 1992; Jansen and Bakke 1993;
Appleby and Mo 1997). Similar data were
obtained by Kanck et al. (2006), who found
highest prevalence and mean intensity of G.
salaris on anadromous Arctic charr in northern
Norway in autumn. Several factors are likely to
affect the seasonal population dynamics of monogenean ectoparasitic infections and may explain
the higher prevalence and abundance of G. salaris
on Arctic charr in autumn. The major abiotic
factor affecting reproduction and population
growth of Gyrodactylus is water temperature, as
it affects the transmission (Soleng et al. 1999) as
well as birth and mortality rates directly and
probably through the host immune system (Scott
and Noakes 1984; Jansen and Bakke 1991;
Andersen and Buchmann 1998). However, the
finding that the G. salaris strain in Pålsbufjorden
performs better on Arctic charr than on Atlantic
salmon (Olstad et al. 2007) may indicate that this
particular G. salaris strain is better adapted to
cold water temperatures (as is Arctic charr
compared to Atlantic salmon). However, the
higher water temperature in August may result
in a higher host resistance than in October (see
Jansen and Bakke 1993). The relatively high
prevalence of infection in October may also relate
to the spawning activity of the charr. Several
studies have shown that reproductive investment
negatively affects the immune response (Deerenberg 1997; Nordling 1998). Accordingly, reduced
immune defense during spawning may result in
higher parasite abundance of G. salaris. In addition, during spawning the charr are more aggregated than during the rest of the year and physical
contact between hosts is more likely. Hence,
parasite transmission rates may be higher (Soleng
et al. 1999). Gyrodactylus salaris in Pålsbufjorden
was more abundant on older than on younger
charr. This pattern can also be explained by
increased physical contact; older fish often have
103
the most aggressive and dominant behavior on
the spawning grounds (Fabricius and Gustafson
1954) and thus face increased risk of getting
infected by contact transmission (Bakke et al.
1992; Petersson and Järvi 1997).
Male charr were significantly higher infected
with G. salaris than females on the spawning
ground in Pålsbufjorden. Male Arctic charr are
known to arrive earlier and stay longer at the
spawning grounds than females (Figenschou et al.
2004) and, thus, encounter a higher probability of
contact transmission. Successive polyandry and
the more aggressive behaviour may further
increase the probability of parasite transmission
through contact. In addition sexually mature
males, in general, face a higher degree of
immuno-suppression than sexually mature females (Skarstein et al. 2001; Ottová et al. 2005).
Increased male reproductive effort may decrease
the individuals’ energy allocation to defense
against disease or parasites (Williams 1966; Sheldon and Verhulst 1996).
A positive correlation between increased
testosterone levels and susceptibility to Gyrodactylus has been shown in salmonids (Buchmann
1997), and this could also potentially contribute to
the observed pattern.
In summary, Arctic charr is apparently a more
common host for G. salaris than previously
expected. Pålsbufjorden and several other lakes
of the Numedalsvassdraget watercourse are infected with viable and persistent G. salaris populations. We conclude that this G. salaris–Arctic
charr association is a stable but perhaps relatively
young parasite-host association. The variation in
prevalence and abundance between late summer
and late autumn and in the different host cohorts,
are interpreted as a result of a combined action of
fluctuations in temperature and seasonal differences in host physiology and ecology. Robertsen
et al. (2007) assumed that the occurrence of G.
salaris on charr in Pålsbufjorden resulted from a
host switch to charr from rainbow trout. Species
and strains closely related to G. salaris are known
to frequently undergo host switching with subsequent reproduction. Since host switches may cause
significant expansions of the geographical range of
pathogenic variants of G. salaris, the frequent
observations of G. salaris on charr have implica-
123
104
tions for the diagnosis, management and control of
salmonid gyrodactylosis.
Acknowledgements We thank Cathrine Vollelv, Henning
Pavels, Guro K. Sandvik, Terje Laskemoen and Bjørn R.
Hansen for help in the field, and Åge Brabrand and Henning
Pavels (Freshwater Ecology and Inland Fisheries
Laboratory, NHM) for background information and help
to determine sex and age of the fish. The project was
supported by the Directorate for Natural Resources
(DN contract nr. 05040026) and the Norwegian Research
Council’s Wild Salmon Programme (Project nr. 145861/
720).
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