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The Parasite Fauna of Rock Ptarmigan (Lagopus muta) in Iceland: Prevalence, Intensity, and Distribution Within the Host Population

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The Parasite Fauna of Rock Ptarmigan (Lagopus muta) in Iceland: Prevalence, Intensity, and Distribution Within the Host Population

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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 zoonotic parasite.
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The Parasite Fauna of Rock Ptarmigan (Lagopus muta) in
Iceland: Prevalence, Intensity, and Distribution Within the Host
Population
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
DOI:
URL: http://www.bioone.org/doi/full/10.1654/4481.1
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The Parasite Fauna of Rock Ptarmigan (Lagopus muta) in Iceland:
Prevalence, Intensity, and Distribution Within the Host Population
KARL SKIRNISSON,
1,3
SOLRUN T. THORARINSDOTTIR,
1
AND OLAFUR K. NIELSEN
2
1
Institute for Experimental Pathology, Keldur, University of Iceland, IS-112 Reykjavik, Iceland (e-mail: karlsk@hi.is,
solrunth@hi.is) and
2
Icelandic Institute of Natural History, Urridaholtsstraeti 6–8, IS-212, Gardabaer, Iceland (e-mail: okn@ni.is)
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
zoonotic parasite.
KEY WORDS: Iceland, rock ptarmigan, Lagopus muta, intestinal helminths, ectoparasites, prevalence, mean intensity,
discrepancy index.
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-
er, 2008).
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)
(Berryman, 2002).
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.
3
Corresponding author.
Comp. Parasitol.
79(1), 2012, pp. 44–55
44
MATERIALS AND METHODS
Ptarmigan sample
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
older).
Hematozoan examination
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.
Gediminas Valkiu
¯nas and Tatjana Jezova, Vilnius Univer-
sity, Lithuania, examined the slides for the presence of
microfilariae and protozoans using standard methods
(Valkiu
¯nas, 2004).
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
2
, 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
A. lagopi.
Mites were mounted in Hoyer’s medium (Gaud and
Atyeo, 1996), and identification was based on Mironov et al.
(2010).
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
detected.
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.
Parasite infection
site and species Group
Geographical occurrence
ReferenceIceland Palaearctic Nearctic
Cardiovascular system
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
Leucocytozoon
lovati (syn. L.
bonasae)
Protozoa no yes yes Clarke, 1938 (after Braun and Willers, 1966);
Hagihara et al., 2004; Holmstad, Hudson,
Vandvik, and Skorping, 2005; Murata et al.,
2007
Leucocytozoon sp. Protozoa no yes yes Stabler et al., 1967
Cardiovascular system,
tissues
Splendidofilaria
papillicerca
(syn. S. smithi)
Nematoda no yes no Bonderenko, 1963 (after Sonin and Barus, 1981);
Holmstad, Hudson, Vandvik, and Skorping,
2005
Splendidofilaria
tuvensis
Nematoda no yes no Sonin and Barus, 1981
Microfilaria sp. Nematoda no yes yes Babero, 1953; Stabler et al., 1967
Intestinal tract
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.,
2006
Eimeria spp. Protozoa yes Brinkmann, 1923; Holmstad, Hudson, and
Skorping, 2005
Coccidia Protozoa yes Watson and Shaw, 1991
Blastocystis sp. Heterontoph yta yes no no This study
Leucochloridium
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
Willers, 1966)
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.)
urogalli
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
Willers, 1966)
Hymenolepis microps Cestoda no yes no Holmstad, Hudson, Vandvik, and Skorping, 2005
Passerilepis
serpentulus
Cestoda yes no no This study
46 COMPARATIVE PARASITOLOGY, 79(1), JANUARY 2012
Parasite infection
site and species Group
Geographical occurrence
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
Barus, 1981)
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);
Huus, 1928
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
Metamicrolichus
islandicus
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
study
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
serpentulus.
Voucher specimens
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
Thorarinsdottir 2007).
Statistical analysis
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).
RESULTS
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.
Endoparasites
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
test, P,0.001).
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
test, P50.06).
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
t-test, P50.29).
Ectoparasites
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
Prevalence
(%)95%cl
No. infected
hosts
Mean
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.
Parasite
species Host* n
Prevalence
(%)95%cl
No. infected
hosts
Mean
intensity 95%cl D
Tetraolichus
lagopi
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
Strelkoviacarus
holoaspis
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
Metamicrolichus
islandicus
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
Myialges
borealis
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
Lagopoecus
affinis
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
Amyrsidea
lagopi
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
Ornithomya
chloropus
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).
Parasite species
Prevalence* Mean intensity*
Frequency distributions of
intensities*
PPP
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%).
DISCUSSION
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
Blastocystis sp.
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-
stood.
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
hosts).
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,
unpublished data).
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.
ACKNOWLEDGMENTS
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-
ing the blood samples.
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SKIRNISSON ET AL.—ROCK PTARMIGAN PARASITES IN ICELAND 55
... Icelandic Rock Ptarmigan (Lagopus muta, hereafter ptarmigan) are an ideal host species to study parasite aggregation because they have been subject to intense research as a game bird and have provided large numbers of replicates for ecological studies (Morrill et al., 2021;Nielsen et al., 2020;Stenkewitz et al., 2016); additionally, their parasite fauna are exceptionally well known and can be sampled with standardized protocols (Skírnisson, Thorarinsdottir & Nielsen, 2012;Stenkewitz et al., 2016). Parasites infecting ptarmigan from a focal population in northeast Iceland comprise a diverse set of ecto-and endoparasites, for which prevalence of several species correlates with host health indices and/or host population densities (Stenkewitz et al., 2016). ...
... In eight of 12 years, sample size was at least 100. Processing of samples and standardized protocols to enumerate parasites are detailed elsewhere (Skírnisson, Thorarinsdottir & Nielsen, 2012;Stenkewitz et al., 2016). However, some salient points bear repeating. ...
... Infective stages of both T. tenuis and the coccidians are likely to be affected by environmental conditions (e.g., humidity). Transmission of C. caudinflata additionally requires an intermediate invertebrate host, the rainworm, the availability of which is dependent on wet conditions (Skírnisson, Thorarinsdottir & Nielsen, 2012). Aggregation levels of the two eimeriid species are also highly temporally dynamic (Þórarinsdóttir, Skírnisson & Nielsen, 2010). ...
Article
Full-text available
Aggregation of macroparasites among hosts is a near-universal pattern, and has important consequences for the stability of host-parasite associations and the impacts of disease. Identifying which potential drivers are contributing to levels of aggregation observed in parasite-host associations is challenging, particularly for observational studies. We apply beta regressions in a Bayesian framework to determine predictors of aggregation, quantified using Poulin’s index of discrepancy ( D ), for 13 species of parasites infecting Icelandic Rock Ptarmigan ( Lagopus muta ) collected over 12 years. 1,140 ptarmigan were collected using sampling protocols maximizing consistency of sample sizes and of composition of host ages and sexes represented across years from 2006–2017. Parasite species, taxonomic group (insect, mite, coccidian, or nematode), and whether the parasite was an ecto- or endoparasite were tested as predictors of aggregation, either alone or by modulating an effect of parasite mean abundance on D . Parasite species was an important predictor of aggregation in models. Despite variation in D across samples and years, relatively consistent aggregation was demonstrated for each specific host-parasite association, but not for broader taxonomic groups, after taking sample mean abundance into account. Furthermore, sample mean abundance was consistently and inversely related to aggregation among the nine ectoparasites, however no relationship between mean abundance and aggregation was observed among the four endoparasites. We discuss sources of variation in observed aggregation, sources both statistical and biological in nature, and show that aggregation is predictable, and distinguishable, among infecting species. We propose explanations for observed patterns and call for the review and re-analysis of parasite and other symbiont distributions using beta regression to identify important drivers of aggregation—both broad and association-specific.
... The species associations we study are Icelandic Rock Ptarmigan (Lagopus muta, hereafter ptarmigan) known to be infected by 17 species of parasite, of which this study focuses on 12 (three endoparasitic species: two nematodes and a coccidian; and nine ectoparasitic species: five mites, three lice, and one fly; Stenkewitz 2017). Details of the chosen parasite species including their taxonomy, life cycle and life history, and degree of specialization are provided elsewhere, as are the rationales for their choice (Skirnisson et al. 2012, Stenkewitz et al. 2016. Briefly, the chosen parasite species were well represented parasitic fauna that could be identified to species (i.e., they were not exceedingly rare parasites, those for which ptarmigan could be considered accidental hosts, or parasites that were insufficiently described taxonomically-for those parasites, see Nielsen et al. 2020). ...
... We provide a brief summary of the study site and methods of bird collection and processing of parasites (details in Skirnisson et al. 2012, Stenkewitz 2017. 1140 ptarmigan were shot in autumns of 2006À2017 at upland sites near Lake M yvatn, in northeast Iceland (65°37 0 N, 17°00 0 W), during the first week of October (Sk ırnisson and Nielsen 2019). ...
... three months old; 50.1% females) and 419 adult birds (one+ years old; 35.8% females) were collected. As stated in Skirnisson et al. (2012), ectoparasites were collected through a combination of filtered vacuuming and direct removal of parasites. Endoparasitic helminths were extracted from the host small intestine and ceca, while coccidian oocysts were quantified from fecal material following the modified McMaster procedure (see Skirnisson et al. 2012). ...
Article
Full-text available
Testing hypotheses in ecological and evolutionary parasitology can require testing whether host traits or coinfecting parasites explain variation in parasitism by focal species. However, when host traits and coinfecting parasites are considered separately, relations between either and parasitism by focal species can be spurious—a problem that is addressed when both are considered together. We assessed whether abundances of focal parasites related to host age/sex and coinfecting parasites for three endoparasites and nine ectoparasites of Icelandic Rock Ptarmigan (Lagopus muta) collected over 12 yr (2006–2017), and quantified the variation in focal parasitism explained by these predictors. Host traits and coinfecting parasites explained significant variation in abundance of all nine focal parasite species for which models converged, when those models were based on groups of parasites sharing tissue tropism and/or transmission pathways and included year as a random effect. We found a single spurious relation: a host age–sex interaction effect that was removed once concurrent parasitism was considered. When considering focal parasites within groups of coinfecting parasites, we found cases of positive, negative, and lacks of correlations. The amount of variation in focal parasite abundance explained by host traits versus coinfecting parasites depended on the focal parasite and its group. Overall variation explained was both related to the prevalence of the focal parasite, possibly due to underlying parasite aggregation, and similar to variation explained in other models in ecology and evolution. We conclude that host traits and coinfecting parasites often combine to determine infection by focal species. Future studies should also explore the mechanisms underlying parasite–parasite relations and their potential impacts on host demography for this and other study associations, and assess relative effects of host traits and coinfecting parasites on focal parasitism.
... Notwithstanding, a brief summary of the methods of bird collection and processing of parasites is provided (cf. Skirnisson et al. 2012, Stenkewitz 2017. ...
... Forty parasite species have been recorded for rock ptarmigan over their geographical range (Skirnisson et al. 2012). As mentioned, sixteen parasites were identified to species. ...
... Detailed parasitological collection and quantification methods can be found in Skirnisson et al. (2012). Briefly, ectoparasites were collected either through filtered vacuuming of ptarmigan carcasses, or a combination of filtered vacuuming and direct removal of parasites from hosts. ...
Article
Measures of parasitism often differ between hosts. This variation is thought due in part to age or sex differences in exposure to parasites and/or susceptibility to parasitism. We assessed how often age or sex biases in parasitism were found using a large, multi‐year (2006 – 2017) dataset of 12 parasite species of Icelandic Rock Ptarmigan (Lagopus muta) . We found host traits (i.e. age and/or sex) accounted for significant variation in abundance of 11 of the 12 parasite species. We often found increased abundance among juvenile hosts, although significant adult biases were observed for three parasite species. Additionally, higher levels of parasitism by many species were observed for female hosts, contrary to frequent male biases in parasitism reported for other vertebrates. Abundance of six parasite species was best explained by interactions between host age and sex; some degree of decrease in abundance with host age was present for both male and female hosts for four of those parasite species. We consider various host and parasite traits that could account for observed singular and repeated patterns of age and/or sex biases in parasitism (e.g. age‐ and sex‐related grouping behaviours, age‐specific mortality in relation to parasitism, acquisition of greater immunity with age). This work provides a foundation for future studies investigating age‐related differences in acquired immunity and age‐specific parasite‐mediated mortality for males and females, as well as studies on interactions between co‐infecting parasite species. This article is protected by copyright. All rights reserved.
... Specifically, few studies are available on the sanitary status of the species, and most of them have been carried out in the northern part of the species range, in Iceland (Skirnisson et al., 2012(Skirnisson et al., , 2016Stenkewitz et al., 2016), Norway (Holmstad et al., 2005) and Japan (Murata et al., 2007;Matsubayashi et al., 2018). On the contrary, the health status of the Rock ptarmigan hasn't been fully investigated in Southern Europe where two subspecies are present at the border of the distribution range: L. muta helvetica and L. muta pyrenaica To our knowledge, this is the first sanitary study carried out on the Pyrenean subspecies (L. ...
... Compared with Fanelli et al. (2020), who have found the Rock ptarmigan living in the Italian Alps free of parasites, this study presents a parasite richness higher than the one detected by Zbdinden and Hoerning (1985) and similar, in terms of different parasite genus, to the one detected by Holmstad et al. (2005) in Norway and Skirnisson et al. (2012) in Iceland. However, a comparison with these studies is difficult, due to the different epidemiological situations of the ptarmigan populations, and due to the distinct population and environmental conditions. ...
Article
Data presented in this work represents the first record of parasites from the Alpine and Pyrenean Lagopus muta subspecies, providing valuable information to consider for conservation management. From 1987 to 2018, 207 Rock ptarmigans were collected in the framework of a long-term sanitary monitoring in France. Eight parasites were found in the Alpine Rock ptarmigan, and one in the Pyrenean subspecies. Only two parasites occurred with high prevalence in the Alpine Rock ptarmigan: Capillaria caudinflata (38.9%) and Eimeria sp. (34.7%). Prevalence of the other parasites (Ascaridia compar, Cestodes, Amphimerus sp. and Trichostrongylus tenuis) was lower than 20%. Dispharynx nasuta was found with a prevalence of 52.9% in the Pyrenean Rock ptarmigan. Overall, we found a spatially aggregated distribution of parasites in the northern French Alps, probably due to both favourable climatic conditions for parasite cycle and high host density. Statistical analyses indicated a positive effect of altitude and latitude on C. caudinflata occurrence whereas risk factors for Eimeria sp. were the distance from urban areas and land cover. In addition, the majority of the infested birds came from areas close to ski-pistes, where human disturbance increases the susceptibility to diseases, causing stress to wildlife.
... nematodes belonging to the genera Oxyspirura, Strongyloides, Syngamus, Amidostomum, and Trichostrongylus, have never been reported to parasitize poultry in Iceland although they are known to occasionally parasitize wild birds in the country. Thus, A. acutum and A. anseris (Skirnisson 2015) are known to occur in anseriform birds and T. tenuis is found in the rock ptarmigan Lagopus muta (Skirnisson et al. 2012) and in domestic and wild geese (Anser anser) (Skírnisson, unpublished). Similarily, acarines that infest poultry in Western Europe such as Argas, Ornithonyssus, Megninia, Dermoglyphus,Columbiphilus and Epidermoptes have never been reported in Iceland. ...
... Moreover, C. obsignata was identified from peridomestic poultry on a farm in Eyjafjörður, North Iceland, and a heavy infection by this species was identified in 2012 in a domestic pigeon Columba livia from the larger Reykjavík area. C. caudinflata is a common parasite of rock ptarmigan (Skirnisson et al. 2012). ...
... Birds used for this analysis were collected specifically for a long-term study on the relation between ptarmigan population change and ptarmigan's health related parameters (Skírnisson et al. 2012, Stenkewitz et al. 2015. To do all the sampling and analysis required for the study at large it was necessary to sacrifice birds. ...
... During dissection, the tail was removed, kept frozen, and later checked for feather holes. Mallophagans were collected according to Skírnisson et al. (2012) using a handheld vacuum cleaner (Princess, Turbo tiger, type 2755). The plumage of the intact bird was vacuum-cleaned for about two min; within this time the whole bird can be vacuumed systematically and thoroughly. ...
Article
Full-text available
Feather holes have traditionally been suggested to be feeding traces of chewing lice (mallophagans). There is controversy whether mallophagans are the real source of feather holes. We studied mallophagan infestations and holes in tail feathers of 528 rock ptarmigan Lagopus muta collected 2007–2012 in northeast Iceland. Three mallophagans were found, Amyrsidea lagopi (prevalence 13%), Goniodes lagopi (72%) and Lagopoecus affinis (51%). The prevalence of feather holes was 15% and based on pattern the holes could be separated into two groups termed feather hole swarms (FHS), prevalence 9%, and single holes (SH), prevalence 6%. Holes for FHS were concentrated in the central tail feathers and decreased outwards, but holes for SH did not show any such pattern. There was a significant positive relationship between the number of holes for FHS birds and A. lagopi number, and the prevalence was similar. No other combinations of FHS or SH and the mallophagans indicated any relationship. The observed differences between FHS and SH suggest that feather holes have different origin. Our thesis based on known feeding habits of amblycerans like A. lagopi is that the holes in FHS are created during the pin feather stage when the lice bite the pin feather to draw blood. The holes in FHS were often in lines parallel to the feather shaft and the distance between adjacent holes was similar to the daily growth band, and where apparent the holes were sitting in the light portion of the band suggesting diurnal rhythm in lice feeding activity. Concluding, feather holes in ptarmigan may have various origins, but there is a clear correlation between the presence and numbers of A. lagopi and FHS. This is a novel finding for the grouse family and the genus Amyrsidea and should be a valuable contribution to the studies of feather hole formation.
... In the present study Cram, 1927Pinto et al., 2004Barus, 1969Barus and Sonin, 1978Barus and Sonin, 1980Baud'huin, 2003 current study that among other galliform birds, the francolins are less prevalent to the helminthic species due to their feeding habits (Millán, 2009;Katoch et al., 2012;Nalubamba et al., 2015;Farooq et al., 2019). Francolins and other galliform birds are more infected by nematodes comparatively, because the nematode eggs are more resistant in the external environment as well as the intermediate host of any type can be a medium of survival for the nematode juveniles, and also because nematodes are less host-specific (Gundy, 1965;Perry, 1989;Pinto et al., 2004;Skirnisson et al., 2012); this is also due to the high amount of arthropod consumption by the host and results in the rate of infection and frequency of nematodes and cestodes found high. It is also observed that birds feed more on insects, get more infected by trematodes, acanthocephalan, and nematodes (Little et al., 1993;Horwitz and Wilcox, 2005;Davies et al., 2008;Macklin and Hauck, 2019;Sarba et al., 2019). ...
Article
Francolins are among the very gregarious variety of game birds severely infected by various parasites that may cause an important source for infection transmission in humans by eating them very fondly in the country. During this study, two commonly found francolins species of the region; Francolinus francolinus (Black Francolin) and F. pondicerianus (Grey Francolin), were examined for helminthes fauna. The study deals with the primary survey of helminthic infection occur in the francolin birds (Phasianidae: Perdicinae) with reference to their forage in gut content. It is the first helminthological and epidemiological study in Sindh, Pakistan. At present, a total of 20 birds were examined, out of which 17 were found infected with cestode larvae of two species of genus Cotugnia and genus Raillietina, one species of trematode, Prosthogonimus potentially new species; one new species of acanthocephalan, Mediorhynchus francolinae sp. nov.; one species of nematode, Subulura brumpti (López-Neyra, 1922) were recovered, with new host records. The forage content and comparative incidence of helminth species were also observed and discussed in the current study, which revealed the high prevalence of infection in grey francolins than that of black francolin. The mean intensity of infection relative to the forage in guts of hosts was found significant (P < 0.05), observed 9.14 ± 1.65 in black francolins than in grey francolins (5.8 ± 0.51). The parasitic abundance was compared using Fisher's Exact Test, which showed no significant difference between cestodes and nematodes in the two hosts, however trematode and acanthocephalan was found only in grey francolin. The parasitic frequencies along with the confidence intervals were recorded higher in black francolins by cestodes and nematodes than the black francolins during the present study.
... The wild birds and poultry that are susceptible to the causative agent of trichostrongyloidosis include Anser albifrons, Anser anser dom., Gallus gallus dom., Anas platyrhynchos dom., Meleagris gallopavo, Anas platyrhynchos, Branta canadensis, Chen caerulescens, Lagopus scoticus, Lagopus muta, Numida meleagris, Otis tarda, Perdix perdix, Pavo cristatus, Phasianus colchicus. Moreover, such a wide distribution of this pathogen in birds is explained by the peculiarities of its development, where exogenous preservation of the parasite at the stages of the egg and larva allows parasites to survive as a species (Watson et al. 1988, Cattadori et al. 2005, Skírnisson et al. 2012). ...
... A complete count of a parasite burden is not always possible. In heavily parasitized hosts, one may restrict the count to only part of the host to reduce the workload involved [22,24]. Parasites such as lice can be hard to isolate so that not all parasites are counted [25]. ...
Article
Aggregation, a fundamental feature of parasite distributions, has been measured using a variety of indices. We use the definition that parasite-host system A is more aggregated than parasite-host system B if any given proportion of the parasite population is concentrated in a smaller proportion of the host population A than of host population B. This leads to indices based on the Lorenz curve such as the Gini index (Poulin's D), coefficient of variation and the Hoover index, all of which measure departure from a uniform distribution. The Hoover index is particularly useful because it can be interpreted directly in terms of parasites and hosts. An alternative view of aggregation is degree of departure from a Poisson (or random) distribution, as used in the index of dispersion and the negative binomial k. These and Lloyd's mean crowding index are reinterpreted and connected back to Lorenz curves. Aggregation has occasionally been defined as the slope from Taylor's law, although the slope appears unrelated to other indices. The Hoover index may be the method of choice when data points are available, and the coefficient of variation when only variance and mean are given.
Article
In the past 25 years, studies on interactions between chewing lice and their bird hosts have increased notably. This body of work reveals that sampling of live avian hosts, collection of the lice, and the aggregated distributions of louse infestations pose challenges for assessing louse populations. The number of lice on a bird varies among host taxa, often with host size and social system. Host preening behavior limits louse abundance, depending on bill shape. The small communities of lice (typically one–four species) that live on individual birds show species-specific patterns of abundance, with consistently common and rare species, and lower year-to-year population variability than other groups of insects. Most species of lice appear to breed continuously on their hosts, with seasonal patterns of abundance sometimes related to host reproduction and molting. Competition may have led to spatial partitioning of the host by louse species, but seldom contributes to current patterns of abundance.
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My motivation in editing this book has been to present as compelling and credible a story as possible. Although I am personally convinced of the soundness of our argument, that food web architecture plays a key role in the cyclic dynamics of many animal populations, I am not sure that others will be so convinced. In this final chapter, therefore, I exercise my prerogative as editor to have the last word, a final attempt to convince the skeptics and to answer the critics.Perhaps the most compelling case comes from the Mikael Münster-Swendsen monumental study of a needleminer infesting Danish spruce forests (chapter 2). Mikael is the only person I know of who has, almost single-handedly, and with considerable precision, measured all the variables suspected of affecting the dynamics of a particular population over an extended period of time (19 years) and in several different localities (seven isolated spruce stands). Others have longer time series from more places, but none has been so complete in terms of the number of variables measured. This exhaustive study enabled him to build a model of the complete needleminer life system, and use this model to home in on the factors responsible for the cyclical dynamics. However, the story would not have been complete without multivariate time series analysis, which led to the discovery of parasitoids as the cause of the key feedback process, density-related reduction in fecundity. The lesson from Münster-Swendsen's work is clear: If we want to understand population dynamics, we need long time series for all the variables likely to affect the dynamics of the subject population(s). In other words, we need to consistently monitor ecological systems over long periods of time and in many different locations. If there is a weakness in his study, it is the absence of the final definitive experiment. Such an experiment would be relatively easy and cheap to do (relative to those described in other chapters), because isolated spruce stands are common in Denmark and parasitoids emerge from the soil a week or two after the needleminer. Thus, parasitoids could easily be excluded by spraying the ground with an insecticide after needleminer emergence.
Article
Nielsen, O. K. & Petursson, G. 1995: Population fluctuations of gyrfalcon and rock ptarmigan: analysis of export figures from Iceland. - Wildl. Biol. 1: 65-71. We analysed harvest data for gyrfalcon Falco rusticolus and rock ptarmigan Lagopus mutus from Iceland with respect to regularity in fluctuations of numbers. The gyrfalcon data concerned live trapped birds exported to Denmark between 1731 and 1793, and totalled 4,848 falcons, including 4,318 grey, 156 half-white and 374 white colour morphs. According to contemporary sources grey birds were part of the local breeding population (islandus-type birds) but the other morphs represented mainly visitors from Greenland. This is also the current situation but some of the lightest Icelandic breeders could be classified as half-white. The rock ptarmigan harvest data concerned birds exported to Europe in the period 1864-1919, in total ca 3.3 million birds. The data series for white and half-white gyrfalcons were significantly correlated (r = 0.501, p < 0.001). The data series for grey and white morphs (r = -0.099, P = 0.445) and grey and the half-white morphs (r = -0.1183, P = 0.360), showed no correlation. Time series analysis showed that the white (candicans-type) morph fluctuated irregularly. The half-white morph behaved similarly but also showed some affinity with the grey morph, and could have represented a mixture of local breeders and Greenlandic winter visitors. Grey morph gyrfalcons and rock ptarmigan showed regular fluctuations in numbers with a 10-year periodicity. The reliance of Icelandic gyrfalcons on rock ptarmigan during the early part of the breeding season and in all phases of the ptarmigan cycle is well established and may offer a case for causal connections between the two cyclic populations.
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Article
The genotype of Blastocystis isolated from humans and animals is highly polymorphic. Therefore, it is important to compare the genotypes of Blastocystis isolates from humans and animals to determine the zoonotic potential of animal isolates. PCR-based genotype classification using known sequence-tagged site (STS) primers allows identification of zoonotic isolates of animal origin. To this end, 51 isolates from monkeys, cattle, pigs, chickens, quails and pheasants were subjected to genotype analysis using seven kinds of STS primers. Out of the 51 isolates, 39 were identified as one of the known genotypes, four showed mixed genotypes, and eight were unknown genotypes as these were negative for all STS primers. When these results were combined with previous studies on 41 isolates from animals and compared with the diversity of genotypes of 102 human Blastocystis hominis isolates, 67.4 % (62/92) of isolates from mammals and birds were identical to human B. hominis genotypes. Since the unknown genotype of human origin had been placed into an additional clade in the small-subunit rRNA gene phylogeny, further molecular study on the eight isolates of unknown genotype from the present study will facilitate our understanding of their zoonotic potential.