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The Parasite Fauna of Rock Ptarmigan (Lagopus muta) in
Iceland: Prevalence, Intensity, and Distribution Within the Host
Author(s) :Karl Skirnisson, Solrun T. Thorarinsdottir, and Olafur K. Nielsen
Source: Comparative Parasitology, 79(1):44-55. 2012.
Published By: The Helminthological Society of Washington
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The Parasite Fauna of Rock Ptarmigan (Lagopus muta) in Iceland:
Prevalence, Intensity, and Distribution Within the Host Population
SOLRUN T. THORARINSDOTTIR,
AND OLAFUR K. NIELSEN
Institute for Experimental Pathology, Keldur, University of Iceland, IS-112 Reykjavik, Iceland (e-mail: firstname.lastname@example.org,
Icelandic Institute of Natural History, Urridaholtsstraeti 6–8, IS-212, Gardabaer, Iceland (e-mail: email@example.com)
ABSTRACT: One hundred rock ptarmigan (Lagopus muta), including 30 each of juvenile males and females, and 20 each of
adult males and females, were collected in October 2006 in northeast Iceland to study their parasite fauna. Fourteen different
parasite species were identified: 6 endoparasites (including the protozoans Eimeria muta,Eimeria rjupa; the heterokontophyt
Blastocystis sp.; the nematodes Capillaria caudinflata and Trichostrongylus tenuis; and the cestode Passerilepis serpentulus)
and 8 ectoparasites (including the feather mites Metamicrolichus islandicus,Strelkoviacarus holoaspis,Tetraolichus lagopi,
and Myialges borealis; the feather lice Goniodes lagopi,Lagopoecus affinis, and Amyrsidea lagopi; and the louse fly
Ornithomya chloropus). Blastocystis sp., P. serpentulus and A. lagopi are new host records. All parasite species showed
aggregated distributions. Six species, E. rjupa,P. serpentulus,M. islandicus,G. lagopi,L. affinis, and O. chloropus, were
more prevalent in juveniles than in adults, and 2 species, Blastocystis sp. and T. tenuis, were more prevalent in adults than in
juveniles. The remaining species did not show age-related differences in prevalence. Blastocystis sp. is the only possible
KEY WORDS: Iceland, rock ptarmigan, Lagopus muta, intestinal helminths, ectoparasites, prevalence, mean intensity,
The Icelandic rock ptarmigan (Lagopus muta)
population has cycles with peak numbers occurring
approximately every 10 yr (Nielsen and Pe´tursson,
1995). The distribution of the rock ptarmigan is
circumpolar Holarctic, in tundra and boreal climatic
zones and mountain regions (Voous, 1960). Similar
10-yr population cycles are known for rock ptarmigan
from other parts of the range, including Alaska,
United States; Northwest Territories, Canada; and
Scotland, United Kingdom (Montgomerie and Hold-
Host–parasite interactions are thought to generate
multiannual cycles in red grouse (Lagopus lagopus
scoticus) in Scotland (Hudson et al., 1998). These
relationships have also been suggested for willow
ptarmigan (Lagopus lagopus lagopus) from Norway
(Holmstad, Hudson, and Skorping, 2005; Holmstad,
Hudson, Vandvik, and Skorping, 2005). Similar
multiannual cycles are known for some populations
of boreal and Arctic herbivores from both sides of the
Atlantic (Keith, 1963). Many believe they are caused
by interactions within food webs, with the agent
being either 1 step below the herbivore in the food
web (plants) or a step above (predators or parasites)
A research project was begun in 2006 to study
population change in rock ptarmigan in Iceland in
relation to parasitic infections and other health-related
questions. Knowledge of the parasite fauna is a
prerequisite for any such study, all the more so since
Holmstad, Hudson, and Skorping (2005) stressed the
importance of using information about the whole
parasite community rather than individual species.
Parasites previously reported for the rock ptarmigan
from Iceland are Eimeria sp., the nematodes
Capillaria caudinflata and Trichostrongylus tenuis,
and the mallophagans Lagopoecus affinis and
Goniodes lagopi (Brinkmann, 1923; Kloster, 1923;
Timmermann, 1950; Skirnisson, 1998). From other
parts of its ranges, a further 24 species of parasites are
known from the rock ptarmigan (Table 1). A different
aspect of the parasite–host relation of the rock
ptarmigan is possible transmission of pathogens to
humans (zoonotic diseases). The rock ptarmigan is
the main game bird in Iceland: up to 150,000 birds
are shot per year (http://www.ust.is/einstaklingar/
veidi/veiditolur-1995-2009/) and, as a consequence,
thousands of people come into contact with freshly
dead ptarmigan each year when dressing the birds.
The purpose of this paper is to describe the
composition of the parasite fauna of the rock
ptarmigan in Iceland. A further goal was to study
how age of host relates to prevalence and intensity of
parasite infections. We also evaluated the possibility
of zoonotic infections by different members of the
rock ptarmigan parasite community.
79(1), 2012, pp. 44–55
MATERIALS AND METHODS
A total of 100 individual rock ptarmigan (hereafter
ptarmigan), 20 adult and 30 juvenile males, and 20 adult and
30 juvenile females, were shot 1–5 October 2006 in
northeast Iceland. The birds were collected out of season
under a license issued by the Icelandic Institute of Natural
History. The study area was located around Lake Myvatn
(65u379N, 17u009W), and most of the birds were collected in
the lava fields and mountains east and north of the lake.
Each bird was tagged immediately after collecting, then
wrapped in absorptive paper, placed in a paper bag, cooled
to 4uC, and transported to the laboratory. All birds were
dissected within 3 d of collection. Birds were sexed using
both the loral stripe and size and color of the combs
(Montgomerie and Holder, 2008) and aged based on
pigmentation of the primaries (Weeden and Watson,
1967). Sex and age were confirmed by inspection of the
gonads and presence of bursas of Fabricius. Two age classes
were recognized: juveniles (birds hatched in 2006, circa 3 mo
old) and adults (birds hatched 2005 and earlier, 15 mo and
Immediately after shooting, 2 blood smears were prepared
from each bird, 1 thin and 1 thick smear (Pritchard and
Kruse, 1982). Slides were air-dried, fixed within a few hours
in methanol, and stored at 4uC until staining with Giemsa.
¯nas and Tatjana Jezova, Vilnius Univer-
sity, Lithuania, examined the slides for the presence of
microfilariae and protozoans using standard methods
Collection and quantification of ectoparasites
The hunters noted, and if possible, collected hippoboscid
flies observed when the bird was being packed (collected
flies were fixed in 70%ethanol). In the laboratory, as each
bird was unwrapped it was visually inspected for hippobos-
cid flies and mallophagans. A hand held vacuum cleaner
(Princess, Turbo tiger, Type 2755) was used to collect
external parasites. The vacuum cleaner was modified for this
purpose; the nozzle (4 31.5 cm) was connected to an
external collection chamber fitted with a circular sack-like
filter (92 cm
, diameter of pores 2–30 mm). Each bird was
vacuumed systematically, covering the whole body in
approximately 1 min. The filter was placed in a plastic
bag and stored at 220uC until analysis.
The contents of the filter, feathers, skin particles, blood
flakes, and parasites, were transferred to a 400-ml glass jar.
The filter was then brushed under a gentle stream of water
on to a glass Petri dish (diameter 100 mm, depth 10 mm).
This mixture was added to the jar, and more water added
until the jar contained approximately 100 ml. Seven drops
of the surfactant TritonHX-100 were added to the jar to
reduce adhesive forces and to promote particle settling.
The jar was fitted with a lid and shaken vigorously by
hand. Feathers were removed 1 by 1 from the mixture and
discarded after being flushed with water over the jar. After
gently stirring to remove air bubbles and particles from the
surface, the sample in the jar was allowed to settle for 1 hr.
Parasites were collected from the sediments under a
stereoscope at 310–35 magnification and preserved in
ethanol. The hippoboscid fly samples included all flies
collected or registered by the hunters as well as flies
detected during processing of the birds. The mallophagan
samples included lice found in the vacuum filters and all
individuals picked manually from the birds or their
wrappings in the lab. Mites were collected exclusively
from the vacuum filters.
Identification of the hippoboscid fly Ornithomya chlor-
opus was based on Theodor and Oldroyd (1964). Identifi-
cation of the mallophagans G. lagopi and L. affinis was
based on Timmermann (1950), and Amyrsidea lagopi on
Scharf and Price (1983). Ricardo L. Palma, Museum of New
Zealand Te Papa Tongarewa, confirmed the identification of
Mites were mounted in Hoyer’s medium (Gaud and
Atyeo, 1996), and identification was based on Mironov et al.
Collection and quantification of endoparasites
The gastrointestinal tract was removed and separated into
the following: (a) esophagus and crop along with trachea
and associated connective tissue; (b) gizzard and glandular
stomach; (c) duodenum; (d) jejunum and ileum; (e) ceca,
separated left and right; and (f) rectum and cloaca
(anatomical terms according to King and McLelland,
1984). Fecal pellets were collected from the rectum. Each
part of the gastrointestinal tract was placed in a plastic bag
and frozen for later analysis.
A sample consisting of 0.5 g of fecal material mixed with
14.5 ml of water was used to study cysts and oocysts of
protozoan parasites as well as eggs of helminths using the
modified McMaster method. Another 0.3 g of fecal material
was analyzed using a fecal parasite concentrator (FPC). The
modified McMaster method gives quantitative values for
oocysts of the different Eimeria spp. (Anonymous, 1986;
Rommel et al., 2000). Values were scaled to oocysts per
gram of feces (opg). The FPC method (Evergreen Scientific,
1998) gives qualitative results and is commonly used to
detect cysts, oocysts, and helminth eggs in feces. The FPC
method enables the detection and morphological studies of
much smaller structures (maximum magnification 31200)
than the McMaster method (maximum magnification
3120). We used the FPC method to study presence/absence
of Blastocystis sp. cysts in each bird. Further, we scored the
number observed under an 18 318 mm coverglass in the
following way: 0 5no Blastocystis detected; 1 51–5 cysts;
256–49 cysts; 3 550–499 cysts; and 4 .than 500 cysts
Both tissues and the individual sections of the alimentary
tract were examined for adult worms. We examined the
connective tissue between the trachea and the esophagus
using a stereoscope at 310 magnification for the nematode
Splendidofilaria papillicerca and examined under the
gizzard membrane for the nematode Amidostomum spp.
Individual sections of the alimentary tract were opened with
a longitudinal incision, and the contents were washed into a
150-mm mesh. After gentle washing with water, the contents
of the mesh were transferred to a Petri dish and examined for
worms under a stereoscope. Worms were counted, fixed in
70%ethanol, and identified to species. Since only 1 of the 2
ceca was analyzed, the worm number was multiplied by 2 to
estimate total number of worms per bird, since worm
numbers do not significantly differ between the 2 cecae
SKIRNISSON ET AL.—ROCK PTARMIGAN PARASITES IN ICELAND 45
Table 1. The parasite fauna of the rock ptarmigan Lagopus muta, infection site, and geographic distribution of the
different parasite species.
site and species Group
ReferenceIceland Palaearctic Nearctic
Trypanosoma avium Protozoa no yes no Haaland, 1925 (after Peirce, 1981)
Trypanosoma sp. Protozoa no yes yes Ellison and Weeden, 1966 (after Braun and
Willers, 1966); Stabler et al., 1967
lovati (syn. L.
Protozoa no yes yes Clarke, 1938 (after Braun and Willers, 1966);
Hagihara et al., 2004; Holmstad, Hudson,
Vandvik, and Skorping, 2005; Murata et al.,
Leucocytozoon sp. Protozoa no yes yes Stabler et al., 1967
(syn. S. smithi)
Nematoda no yes no Bonderenko, 1963 (after Sonin and Barus, 1981);
Holmstad, Hudson, Vandvik, and Skorping,
Nematoda no yes no Sonin and Barus, 1981
Microfilaria sp. Nematoda no yes yes Babero, 1953; Stabler et al., 1967
Eimeria brinkmanni Protozoa no no yes Levine, 1953
Eimeria fanthami Protozoa no no yes Levine, 1953
Eimeria lagopodi Protozoa no yes no Galli-Valerio, 1929
Eimeria muta Protozoa yes no no Skirnisson and Thorarinsdottir, 2007
Eimeria rjupa Protozoa yes no no Skirnisson and Thorarinsdottir, 2007
Eimeria Type B Protozoa no yes no Ishihara et al., 2006
Eimeria uekii Protozoa no yes no Kamimura and Kodama, 1981; Ishihara et al.,
Eimeria spp. Protozoa yes Brinkmann, 1923; Holmstad, Hudson, and
Coccidia Protozoa yes Watson and Shaw, 1991
Blastocystis sp. Heterontoph yta yes no no This study
variae (syn. L. pricei)
Trematoda no no yes Babero, 1953; Jellison and Neiland, 1965;
Weeden 1965 (after Braun and Willers, 1966)
Brachylaema fuscata Trematoda no no yes Babero, 1953; DeLeonardis, 1952, unpublished
thesis, University of Alaska, Fairbanks (after
Braun and Willers, 1966); Jellison and
Neiland, 1965; Weeden, 1965 (after Braun and
Davainea proglottina Cestoda no no yes Babero, 1953; DeLeonardis, 1952, unpublished
thesis, University of Alaska, Fairbanks (after
Braun and Willers, 1966); Weeden, 1965 (after
Braun and Willers, 1966)
Paroniella (R.) (D.)
Cestoda no yes yes Babero, 1953; Holmstad, Hudson, Vandvik, and
Skorping, 2005; Huus, 1928; Jellison and
Neiland, 1965; Watson and Shaw, 1991;
Weeden, 1965 (after Braun and Willers, 1966)
Haploparaxis galli Cestoda no no yes Babero, 1953; DeLeonardis, 1952, unpublished
thesis, University of Alaska, Fairbanks (after
Braun and Willers, 1966); Jellison and
Neiland, 1965; Rausch, 1951 (after Braun and
Willers, 1966); Weeden, 1965 (after Braun and
Hymenolepis microps Cestoda no yes no Holmstad, Hudson, Vandvik, and Skorping, 2005
Cestoda yes no no This study
46 COMPARATIVE PARASITOLOGY, 79(1), JANUARY 2012
site and species Group
ReferenceIceland Palaearctic Nearctic
Metroliasthes sp. Cestoda no no yes DeLeonardis, 1952, unpublished thesis,
University of Alaska, Fairbanks (after Braun
and Willers 1966)
Rhabdometra nullicollis Cestoda no no yes Babero, 1953; Jellison and Neiland, 1965;
Weeden, 1965 (after Braun and Willers, 1966)
Amidostomum acutum Nematoda no yes no Mamaev , 1959 (after Sonin and Barus, 1981)
Trichostrongylus tenuis Nematoda yes yes yes Holestad et al., 1994; Holmstad, Hudson,
Vandvik, and Skorping, 2005; Watson and
Shaw, 1991; Weeden, 1965 (after Braun and
Willers, 1966), this study
Ornithostrongylus sp. Nematoda no yes no Gubanov and Nakhodkina, 1971 (after Sonin and
Heterakis gallinarum Nematoda no yes yes Boughton, 1935, unpublished thesis, University
of Minnesota, St. Paul (after Braun and
Willers, 1966); Boughton, 1937 (after Braun
and Willers, 1966); Cram, 1927 (after Braun
and Willers, 1966); Galli-Valerio, 1931;
Shipley, 1909 (after Sonin and Barus, 1981)
Ascaridia compar Nematoda no yes yes Babero, 1953; Cerutti et al., 2008; Cram, 1927
(after Braun and Willers, 1966); Holmstad,
Hudson, Vandvik, and Skorping, 2005; Sonin
and Barus, 1981; Weeden, 1965 (after Braun
and Willers, 1966)
Ascaridia galli Nematoda no no yes DeLeonardis, 1952, unpubl ished thesis,
University of Alaska, Fairbanks (after Braun
and Willers, 1966)
Ascaridia sp. Nematoda no yes yes Bonderenko, 1963 (after Sonin and Barus, 1981);
Capillaria caudinflata Nematoda yes yes no Brinkmann, 1923; Holmstad, Hudson, Vandvik,
and Skorping, 2005; Huus, 1928; Kloster,
1923; this study
Capillaria sp. Nematoda yes Babero, 1953
Thoracic cavity, air sacks
Diplotriaena counturieri Nematoda no yes no Dollfus, 1956 (after Sonin and Barus, 1981)
Plume or skin
Strelkoviacarus holoaspis Astigmata yes no no Mironov et al., 2010; this study
Tetraolichus lagopi Astigmata yes no no Mironov et al., 2010; this study
Astigmata yes no no Mironov et al., 2010; this study
Myialges borealis Astigmata yes no no Mironov et al., 2010; this study
Mironovia lagopi Prostigmata yes no no Bochkov and Skirnisson, (2011), this study
Goniodes lagopi Phthiraptera yes yes yes Harper, 1953; Holmstad 2004, unpublished
thesis, University of Bergen, Norway; Mehl,
1975; Steen, 1978; Timmermann, 1950; this
Lagopoecus affinis Phthirapt era yes yes yes Harper , 1953; Holmstad, 2004, unpublished
thesis, University of Bergen, Norway; Jellison
and Neiland, 1965; Mehl, 1975; Steen, 1978;
Timmermann, 1950; this study
Amyrsidea lagopi Phthiraptera yes no no this study
Ceratophyllus garei Siphonaptera yes yes no Mehl, 1975; Steen, 1978; this study
Ornithomya chloropus Diptera yes yes no Mehl, 1975; Steen, 1978; this study
Table 1. Continued.
SKIRNISSON ET AL.—ROCK PTARMIGAN PARASITES IN ICELAND 47
(Wilson, 1979, unpublished thesis, University of Aberdeen,
Scotland; Wilson, 1983). Identification of nematodes was
based on Madsen (1945), Wehr (1971), and McDonald
(1974), while Alexander Galkin of the Russian Academy of
Sciences, St. Petersburg, identified the cestode Passerilepis
The following specimens were deposited in the
Icelandic Institute of Natural History, Gardabaer, Iceland:
P. serpentulus (catalog accession number NI-4559, LM-
06-047), T. tenuis (NI-4560, LM-06-027), C. caudinflata
(NI-4561, LM-06-210), G. lagopi (NI-4562, LM-06-166),
L. affinis (NI-4563, LM-06-073), A. lagopi (NI-4564, LM-
06-075), and O. chloropus (NI-4565, LM-06-010). Type
material of Tetraolichus lagopi,Strelkoviacarus holoaspis,
Metamicrolichus islandicus, and Myialges borealis was
deposited in the Museum of Zoology, University of
Michigan, Ann Arbor, United States, and the Zoological
Institute of the Russian Academy of Sciences, St.
Petersburg, Russia (details in Mironov et al. 2010).
Photosyntypes of sporulated Eimeria muta and Eimeria
rjupa oocysts were deposited in U.S. National Parasite
Collection, Beltsville, Maryland (details in Skirnisson and
Count data existed for 13 of 14 species of ptarmigan
parasites observed. This included the total number of
parasites in or on the host for 3 worms and the hippoboscid
fly, and indexes of abundance for 2 eimerids, 4 mites, and 3
mallophagans. For 1 species, Blastocystis sp., only ordinal
density values were obtained.
Descriptive statistics, prevalence of infection, mean
intensity of infection, and discrepancy index were calculated
for each parasite species for total sample and subdivided
according to host age. Prevalence of infection is percentage
of hosts infected with the parasite; mean intensity of
infection is the mean number of parasites per host in
infected individuals only. The Sterne method was used to
calculate the 95%confidence limits for prevalence, and the
bootstrap method for confidence limits for mean intensity
(Ro´zsa et al., 2000). We calculated the index of discrepancy
to study dispersion of parasites within the host population
(Poulin, 1993). The discrepancy index ranges between 0 and
1, high values indicate aggregated distribution and low
values a uniform distribution.
Fisher’s exact test was used to compare prevalence, and a
bootstrap t-test and a Brunner–Munzel test to compare mean
intensity among host age groups (Ro´zsa et al., 2000). Same
tests were used when comparing prevalence and mean
intensity among different parasite species. Mood’s median
test was used when species being compared for median
intensity were more than 2. To compare the frequency
distributions of parasite intensities, a bootstrap test of
stochastic equality was used (Reiczigel et al., 2005).
Comparison of mean intensity and frequency distributions
of intensities were not done where sample sizes were less
than 5 in a group (T. tenuis and A. lagopus). The alpha level,
2-tailed, was set at P50.05 for all tests. All statistical
analyses were performed using the program Quantitative
Parasitology (Ro´zsa et al., 2000).
The parasite fauna
Six endoparasite and 8 ectoparasite species were
observed in the ptarmigan. Prevalence and intensity
data are presented in Tables 2 and 3 for endoparasites
and ectoparasites, respectively. The results of statis-
tical comparisons of host age-related differences in
prevalence, mean intensity, and frequency distribu-
tions of intensities are presented in Table 4. No blood
or tissue parasites were found.
The coccidians E. muta and E. rjupa and the
heterokontophyt Blastocystis sp. were found in fecal
material. Specimens of E. muta were very common;
prevalence was 92%and mean intensity 8,580 opg.
Neither prevalence nor mean intensity showed a
significant host age-related difference, but frequency
distribution of intensities did. This difference was
also apparent in the discrepancy index (Table 2); E.
muta was more aggregated in adult hosts. Prevalence
of E. rjupa was 26%, and mean intensity was
8,190 opg. Prevalence was significantly lower for
adult hosts (13%) than juvenile hosts (35%), but
there was no significant difference in either mean
intensity or frequency distribution of intensities. Both
Eimeria species showed an aggregated distribution
within the host population, but this was much more
pronounced for E. rjupa (Table 2). There was no
significant difference in mean intensity among the 2
eimerids (bootstrap t-test, P50.75), but prevalence
was significantly higher for E. muta (Fisher’s exact
Blastocystis sp. cysts have not previously been
reported from ptarmigan. They were morphologically
similar to those reported for humans (Ash and Orihel,
1997). The prevalence of Blastocystis sp. was very
high, 91%. There was a significant host age-related
difference in Blastocystis sp. prevalence: all adults
were infected, but prevalence in juveniles was 85%.
Only ranked values exist for mean intensity of
Blastocystis infections, and these data indicated no
difference among host age groups (Brunner–Munzel
The tapeworm P. serpentulus and the nematode C.
caudinflata were found in the first third of the small
intestine. The prevalence of P. serpentulus was only
3%, and a mean intensity of 18.0 worms per bird was
found only in juvenile hosts. The prevalence of C.
caudinflata was 33%, and mean intensity was 17.1
worms per bird. There was no host age-related
48 COMPARATIVE PARASITOLOGY, 79(1), JANUARY 2012
difference in prevalence, mean intensity, or frequency
distribution of intensities. The nematode T. tenuis
was found in the ceca, the prevalence was 14%, and
mean intensity was 3.4 worms per bird. There was a
significant difference among host age groups in
prevalence of T. tenuis infections (Table 4). For adult
hosts prevalence was 30%and for juvenile hosts 3%.
All 3 species of worms showed an aggregated
distribution (Table 2). There was a significant
difference in prevalence of the 2 nematode species,
C. caudinflata being more prevalent (Fisher’s exact
test, P50.002) but not in mean intensity (bootstrap
Four species of mites were found in the vacuum
filter, only 1 of them, the vane mite T. lagopi, was
also observed in situ (mites microhabitats sensu
Dabert and Mironov, 1999). It was usually densely
packed between barbs, close to the shaft (rachis) of
the primary under wing coverts. In heavy infections it
was also detected on the alula. The prevalence of the
down mite S. holoaspis was 37%, and mean intensity
was 34.6 mites per bird. There was no host age-
related difference for S. holoaspis infections with
respect to prevalence, mean intensity, or frequency
distribution of intensities. The prevalence of the skin
mite M. islandicus was 35%, and mean intensity was
12.9 mites per bird. There was a host age-related
difference both with respect to prevalence and
intensity of M. islandicus infections, but not with
respect to frequency distribution of intensities.
Prevalence was 18%for adult hosts and 47%for
juvenile hosts, and mean intensity 2.9 for adults and
15.4 mites per bird for juveniles. The prevalence of
the skin mite M. borealis was 20%, and mean
intensity was 2.1 mites per bird. There was no
significant age-related difference of M. borealis
infections in prevalence, mean intensity, or frequency
distribution of intensities. The prevalence of T. lagopi
was 92%, and mean intensity was 16.1 mites per bird.
There was no significant age-related difference of T.
lagopi infections with respect to prevalence, mean
intensity, or frequency distribution of intensities.
There was a significant difference in prevalence of
the 4 mite species (Fisher’s exact test, P,0.001). T.
lagopi was the most prevalent, then S. holoaspis and
M. islandicus, with M. borealis the least prevalent.
There was also a significant difference in median
intensity among the 4 species (Mood’s median test, P
,0.001). The heaviest infections were found for T.
lagopi, then S. holoaspis,M. islandicus, and M.
borealis. All 4 mites showed an aggregated distribu-
tion among the hosts (Table 3).
Feather lice were observed primarily on the head
and the upper neck region, but also on the wings and
Table 2. Endoparasites from rock ptarmigan Lagopus muta in northeast Iceland: species, host age groups, sample
size (n), prevalence, 95%confidence limits (95%cl), number of infected hosts, mean intensity, and discrepancy index
(D). Intensities for E. muta and E. rjupa are oocysts per gram feces, and for P. serpentulus,T. tenuis, and C.
caudinflata, worms per bird.
Parasite species Host* n
intensity 95%cl D
Eimeria muta All 100 92 85–96 92 8,578 5,298–19,115 0.706
Juv 60 97 89–99 58 6,910 5,170–9287 0.573
Ad 40 85 70–93 34 11,425 2780–39,401 0.823
Eimeria rjupa All 100 26 18–35 26 8,189 3,881–17,334 0.933
Juv 60 35 24–48 21 9,167 4,002–19,422 0.902
Ad 40 13 5–26 5 4,082 42–12,040 0.949
Blastocystis sp. All 100 91 83–95 91 — — —
Juv 60 85 74–92 51 — — —
Ad 40 100 92–100 40 — — —
Passerilepis serpentulus All 100 3 1–8 3 18 1.0–34.7 0.979
Juv 60 5 1–35 3 18 — —
Ad 40 0 — 0 0 — —
Trichostrongylus tenuis All 100 14 8–22 14 3.4 2.6–4.6 0.891
Juv 60 3 1–11 2 3.0 — 0.956
Ad 40 30 17–46 12 3.5 2.5–4.8 0.770
Capillaria caudinflata All 100 33 24–43 33 17.1 7.9–42.0 0.915
Juv 60 32 21–45 19 9.5 5.3–15.8 0.861
Ad 40 35 21–51 14 27.4 6.4–96.9 0.911
* Juv 5juvenile; Ad 5adult.
SKIRNISSON ET AL.—ROCK PTARMIGAN PARASITES IN ICELAND 49
Table 3. Ectoparasites from rock ptarmigan Lagopus muta in northeast Iceland: species, host age groups, sample
size (n), prevalence, 95%confidence limits (95%cl), number of infected hosts, mean intensity, and discrepancy index
(D). Intensities for T. lagopi,S. holoaspis,M. islandicus, and M. borealis are individuals collected in filter by
vacuuming ,1 min per host, for G. lagopi,L. affinis,A. lagopi, and O. chloropus same procedure as above plus
individuals collected manually during processing of host.
species Host* n
intensity 95%cl D
All 100 92 85–96 92 16.1 12.9–20.8 0.572
Juv 60 95 86–99 57 16.1 12.5–21.3 0.511
Ad 40 88 74–95 35 16.2 10.5–26.1 0.637
All 100 37 28–47 37 34.6 21.8–57.5 0.866
Juv 60 40 28–53 24 23.8 14.4–41.0 0.824
Ad 40 33 20–49 13 54.6 24.3–111.5 0.866
All 100 35 26–45 35 12.9 7.6–21.4 0.877
Juv 60 47 34–59 28 15.4 9.0–25.0 0.823
Ad 40 18 8–32 7 2.9 1.4–4.3 0.868
All 100 20 13–29 20 2.1 1.5–2.8 0.860
Juv 60 25 16–37 15 2.3 1.6–3.2 0.822
Ad 40 13 5–26 5 1.4 1.0–1.8 0.882
Goniodes lagopi All 100 81 72–88 81 14.9 11.5–20.0 0.635
Juv 60 98 91–100 59 15.9 11.9–22.4 0.548
Ad 40 55 39–70 22 12.1 7.6–21.0 0.743
All 100 52 42–62 52 3.6 2.8–5.0 0.710
Juv 60 65 52–76 39 3.4 2.5–5.4 0.656
Ad 40 33 20–49 13 4.0 2.8–5.5 0.765
All 100 10 5–17 10 10.1 4.5–20.3 0.944
Juv 60 13 6–25 8 11.6 5.0–23.5 0.922
Ad 40 5 9–17 2 4.0 — 0.927
All 100 33 24–43 33 2.4 1.9–2.8 0.764
Juv 60 42 30–55 25 2.4 1.8–2.9 0.704
Ad 40 20 9–35 8 2.4 1.6–3.1 0.831
* Juv 5juvenile; Ad 5adult.
Table 4. Comparison of parasite prevalence, mean intensity and frequency distribution of intensities among rock
ptarmigan Lagopus muta host age groups, adults versus juveniles, in northeast Iceland. The results are given as 2-
tailed probability values (P).
Prevalence* Mean intensity*
Frequency distributions of
Eimeria muta 0.057 0.551 0.015
Eimeria rjupa 0.019 0.367 0.275
Blastocystis sp. 0.010 — —
Trichostrongylus tenuis 0.001 — —
Capillaria caudinflata 0.829 0.428 0.992
Tetraolichus lagopi 0.261 0.806 0.253
Strelkoviacarus holoaspis 0.528 0.364 0.499
Metamicrolichus islandicus 0.003 0.026 0.198
Myialges borealis 0.201 0.165 0.201
Goniodes lagopi 0.001 0.382 0.317
Lagopoecus affinis 0.002 0.560 0.113
Amyrsidea lagopi 0.308 — —
Ornithomya chloropus 0.030 0.969 0.992
* Fisher’s exact test was used to compare prevalence, a bootstrap t-test to compare mean intensity, and a bootstrap test of stochastic equality
to compare frequency distributions (Ro´ zsa et al., 2000; Reiczigel et al., 2005). Comparisons of mean intensity and frequency distribution of
intensities were not done for Blastocystis sp. as only ordinal data existed, and T. tenuis and A. lagopi as sample sizes were small (n,5ina
group). No tests were done for Passerilepis serpentulus since it was only found in juvenile hosts.
50 COMPARATIVE PARASITOLOGY, 79(1), JANUARY 2012
the body. The feather louse G. lagopi was very
common; prevalence was 81%, and mean intensity
14.9 lice per bird. A significant age-related difference
was found for prevalence of G. lagopi infections, but
not for mean intensity or frequency distribution of
intensities. Prevalence for G. lagopi was 55%for
adult hosts but 98%for juveniles. The feather louse
L. affinis was also common, prevalence was 52%,
and mean intensity was 3.6 lice per bird. There was a
significant difference in prevalence of L. affinis
contrasting adult hosts and juveniles, but not in mean
intensity or frequency distribution of intensities.
Prevalence for adult hosts was 33%, and for juvenile
hosts it was 65%. The feather louse A. lagopi was the
least common of the 3, prevalence was 10%, and
mean intensity was 10.1 lice per bird. There was no
host age-related difference of A. lagopi infections
with regard to prevalence, mean intensity, or
frequency distribution of intensities. All 3 feather
lice species showed an aggregated distribution
(Table 3). There was a significant difference in
prevalence among the 3 species (Fisher’s exact test,
P,0.001); G. lagopi was the most prevalent, then L.
affinis, and finally A. lagopi. The difference in
median intensity–G. lagopi 8.0, L. affinis 2.5, and A.
lagopi 4.5 lice per bird–was also significant (Mood’s
median test, P,0.001).
The hippoboscid fly O. chloropus was found in the
plume of the host. Prevalence was 33%, and mean
intensity 2.4 flies per bird. Ornithomya chloropus
showed an aggregated distribution (Table 3). There
was a significant host age-related difference in O.
chloropus infections with respect to prevalence, but
not mean intensity or frequency distribution of
intensities. Juvenile hosts had higher prevalence of
O. chloropus than adults (42%vs. 20%).
Fourteen parasite species were observed in this
study, including 3 new host records: Blastocystis sp.,
the tapeworm P. serpentulus, and the mallophagan A.
lagopi. Previously and based on the same data set, 6
species new to science were described, including the
2 eimerids (Skirnisson and Thorarinsdottir, 2007;
Thorarinsdottir et al., 2010) and the 4 astigmatid
mites (Mironov et al., 2010). Altogether, this makes 9
new host records. The other 5 species were known
ptarmigan parasites (Table 1), including 2 nematodes
(T. tenuis and C. caudinflata), 2 mallophagans (G.
lagopi and L. affinis), and the louse fly (O.
chloropus). Since 2006, 2 more species have been
added to the list of ptarmigan parasites in Iceland.
One is the flea Ceratophyllus garei, a known
ptarmigan parasite from other areas (Table 1), and a
common parasite of ground-nesting birds in Iceland
(Henriksen, 1939; Karl Skirnisson, unpublished
data). The identification was confirmed by Robert
E. Lewis, Iowa State University, United States. The
other parasite, the tenth new host record detected in
Iceland, is Mironovia lagopus, a prostigmatid quill
mite, of the family Syringophilidae (Bochkov and
Skirnisson, 2011). Thus, in total 16 parasites have
been reported from the ptarmigan in Iceland. Twenty-
four more species can be added to the list of
ptarmigan parasites from other parts of the range,
all of them are endoparasites (Table 1). Four of those
species are confined to the cardiovascular system: the
sporozoan Leucocytozoon lovati, the flagellate Try-
panosoma sp., and the larvae of the tissue nematodes
Splenditofilaria papillocerca and Splenditofilaria
tuvensis. The adult Splendidofilaria nematodes live
within the connective tissue that connects the trachea
and the esophagus. Eighteen species are confined to
the gizzard and the intestinal tract: 5 species of
Eimeria,E. brinkmanni,E. fanthami,E. lagopodi,E.
uekii, and Eimeria Type B; 2 species of trematodes,
Leucochloridium variae and Brachylaima fuscata;6
species of tapeworms, Davainea proglottina,Haplo-
paraxis galli,Hymenolepis microps,Paroniella
urogalli,Metroliasthes sp., and Rahbdometra nulli-
collis; and 5 species of nematodes, Amidostomum
acutum,Ascaridia compar,Ascaridia galli,Heterakis
gallinarum, and Ornithostrongylus sp. One nema-
tode, Diplotriaena counturieri, infects the air sacs.
It is of interest to note the complete absence of
hematozoan parasites from ptarmigan in Iceland and
a greatly impoverished helminth fauna. Various
factors could be responsible for this pattern. A likely
explanation is a founder effect and lack of suitable
intermediate hosts in Iceland. The source population
of the Icelandic ptarmigan is Greenland (Montgom-
erie and Holder, 2008). No studies have been done on
the parasite fauna of the Greenland rock ptarmigan. A
priori one would expect the Icelandic rock ptarmigan
parasite fauna to reflect the Greenland fauna, i.e.,
absence of hematozoan parasites and impoverished
helminth fauna. Also, successful colonization of
parasites with complicated life cycles, i.e., the
hematozoans, cestodes, and trematodes (cf. Table 1),
should be contingent on the presence of suitable hosts
within Iceland, both with regard to final hosts (i.e.,
Culicoides midges) as well as intermediate hosts (i.e.
certain terrestrial snails or grasshoppers). Neither
Culicoides midges nor grasshoppers are found in
SKIRNISSON ET AL.—ROCK PTARMIGAN PARASITES IN ICELAND 51
Iceland (Olafsson, 1991), and some of the snails
known to be intermediate hosts for helminths
parasitizing rock ptarmigan are not found in Iceland
(Einarsson, 1977). Consequently, such parasites—
even though they had been carried over by the
founders—should be unable to thrive in Iceland. The
absence of mite infections in ptarmigan outside of
Iceland is best explained by sampling methods.
Parasitologists working with rock ptarmigan have
ignored or not found these species previously. It is
expected that the same or related species will be
found occupying the same host habitats in other rock
ptarmigan populations. The same should apply to
The prevalence of infection of the different parasite
species observed in this study fell into 3 main groups
with respect to host age:
(1) No difference in prevalence (6 species, E.
muta,C. caudinflata,S. holoaspis,M. bor-
ealis,T. lagopi, and A. lagopi).
(2) Higher prevalence in juveniles (6 species, E.
rjupa,P. serpentulus,M. islandicus,G.
lagopi,L. affinis, and O. chloropus).
(3) Higher prevalence in adult birds (2 species,
Blastocystis sp. and T. tenuis).
These age-related infection patterns depend on a
variety of factors. Most of them are poorly under-
Two of the 6 species that showed no relation to
host age, the mites T. lagopi and S. holoaspis, do not
come into direct contact with the living tissues of the
host since they live on feathers and in down
(Mironov, 1999). Some authors regard such feather
mites as commensals rather than parasites (Bush et
al., 2001). The supposed benefit for the host is
removal of excess waxes, dirt, and bacteria by the
feeding mites. If commensalism were the case, one
would expect to find a high prevalence of infection
across all age groups. Of the 2 species, T. lagopi was
more widely distributed in the samples than S.
holoaspis. The other 4 species, E. muta,C. caudin-
flata,M. borealis, and A. lagopi, come into contact
with living tissues of the host and should elicit a
response from the immune system and, furthermore,
M. borealis is 1 of the 2 likely candidates for mange
in ptarmigan. That there are no prevalence differences
between host age groups suggests a limited ability of
the host immune system to control those 4 parasites.
For the 6 species the only significant difference in
either mean intensity or the frequency distributions of
intensities was for E. muta (more aggregated on adult
A higher prevalence of infection in juvenile hosts
was found in 6 of 14 species. All these parasites,
except the ischnocerid mallophagans G. lagopi and L.
affinis, come into contact with live tissues of the host.
These 2 mallophagans feed on feathers (Clayton et
al., 2008). This pattern, high host juvenile prevalence,
suggests that host defenses (immune system, preen-
gland activity, and preening behavior) (Bush et al.,
2001) are less well developed in juveniles than in
adults. A lower prevalence of infections, as juvenile
birds mature into adults, might be the result of host
defenses or selective mortality (Hudson et al., 1992;
Schei et al., 2005). Only 1 of the 6 species showed a
significant difference in mean intensity of infection
(M. islandicus higher mean intensity in juveniles), but
none showed a significant difference in the frequency
distributions of intensities.
The least common pattern, found in 2 parasite
species, was for higher prevalence among adult hosts.
For T. tenuis this pattern is well known for red grouse in
Scotland and relates to longevity of the parasite and
accumulated infections (Wilson, 1979, unpublished
thesis, University of Aberdeen, Scotland; Wilson,
1983). Adult red grouse also had higher mean
intensities of infection. The case for Blastocystis sp.
is more puzzling; it is a short-lived unicellular organism
and shows a very high prevalence of infection. In adult
hosts the prevalence was 100%, and in juvenile hosts it
was 85%. It is not clear why this parasite should be
more prevalent in adults than juveniles.
Three of the 14 parasites found in this study have
indirect life cycles with the ptarmigan as the final
host. Two of these cases are of interest: P.
serpentulus where cysticercoids have been found in
coleopteran insects (Procopic
ˇ, 1967) and C. caudin-
flata where earthworms (oligochaetes), obligate
intermediate hosts in the life cycle, act as the source
of infection (Morehouse, 1942, unpublished thesis,
Iowa State College, Iowa; Moravec et al., 1987;
Rommel et al., 2000). A variety of invertebrates,
including earthworms, form a significant part of the
diet of a growing ptarmigan chick in Iceland, whereas
invertebrates are not prominent in the diet of adult
ptarmigan (Gardarsson, 1971, unpublished thesis,
University of California, Berkeley). These observa-
tions on diet support the prevalence of P. serpentulus
in this study; all infections were confined to
juveniles. The short-lived cestode disappears within
a few months, and reinfections do not occur as the
juveniles shift to a vegetarian adult diet. On the other
hand, C. caudinflata does not fit this pattern of
invertebrate-phagous juvenile hosts being predomi-
52 COMPARATIVE PARASITOLOGY, 79(1), JANUARY 2012
nantly infected. In the autumn, both host age groups
were equally infected by C. caudinflata. Since
observations suggest that the lifespan of adult C.
caudinflata worms is less than 5 mo (Morehouse,
1942, unpublished thesis, Iowa State College, Iowa),
this indicates that infections are acquired during
summer at a similar rate by both adults and juveniles.
Extant studies on food habits of adult ptarmigan in
summer have failed to record earthworms (Gardars-
son, 1971, unpublished thesis, University of Califor-
nia, Berkeley). Therefore, it remains unknown how
adult ptarmigans infected with C. caudinflata in
autumn have acquired their infections. One possibil-
ity is that infective larvae originating from decom-
posed earthworms are accidentally being ingested
with water or food.
Some ptarmigan parasites are known to be patho-
genic. Eimeria spp. cause coccidiosis (Rommel et al.,
2000), T. tenuis causes strongylosis or ‘‘grouse
disease’’ (Lovat, 1911), and Epidermoptidae skin
mites are known to cause mange in birds (Mironov,
1999; Gilardi et al., 2001). The only parasitic disease
observed in the birds sampled and examined in the
present study was mange, likely caused by M.
islandicus. The observed densities of T. tenuis were
much lower than required to cause strongylosis
(Hudson, 1986). No signs of coccidiosis were found
in this study, but this disease has been observed in
radio-tagged ptarmigan in Iceland that were found
dead during early winter when birds were heavily
infected with E. muta (opg values up to 227,000,
The protozoan Blastocystis sp. is possibly zoonotic
(Yoshikawa et al., 2004; Tanizaki et al., 2005). In
some humans Blastocystis sp. is known to cause
abdominal discomfort and diarrhea (Ash and Orihel,
1997). This parasite has been confirmed in humans in
Iceland, although it is rare (Skirnisson et al., 2003).
Our studies on the parasite fauna of rock ptarmigan
have delivered new information, including 10 new
host records (this study, Skirnisson and Thorarins-
dottir, 2007; Mironov et al., 2010; Bochkov and
Skirnisson, 2011). In this paper we give the first
description of the distribution within the host
population of 9 of those species. Further, our studies
show that an important group of ectoparasites, the
mites, has been more or less totally ignored in earlier
work on rock ptarmigan parasites. This is all the more
important since 1 of these mites, M. islandicus,is
believed to cause mange in rock ptarmigan. This gap
in the knowledge of the ectoparasite fauna also
applies to all other grouse (Tetraonidae) species.
This study was funded by the Icelandic Centre for
Research (grant number 090207021), the Research
Fund of the University of Iceland, and the Icelandic
Institute of Natural History. We would like to thank
the Lake Myvatn Nature Research Station (RAMY)
and the Northeast Iceland Nature History Office for
logistical support. We are grateful to the hunters
Adalsteinn O. Snaethorsson, Finnur L. Johannsson,
Gudmundur A. Gudmundsson, Thorkell L. Thorar-
insson, and Thorvaldur Th. Bjornsson for collecting
the ptarmigan. We thank Eric P. Hoberg, Jeno
Reiczigel, and 2 anonymous reviewers for valuable
comments on the manuscript; the experts Andre V.
Bochkov, Alexander Galkin, Robert E. Lewis, Sergey
V. Mironov, and Ricardo L. Palma for invaluable
help by describing or confirming identifications of
some of the parasites detected in the survey; and
Tatjana Jezova and Gediminas Valkiu
¯nas for analyz-
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