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The relationship between parasites and spleen and bursa mass in the Icelandic Rock Ptarmigan Lagopus muta

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The spleen and bursa of Fabricius in birds are organs that play an important role in fighting parasite infections. The size of these organs can be used by ecologists as a measure of immune investment, with larger size implying greater investment. The bursa only occurs in juvenile birds during the development of the B cell repertoire, whereas the spleen, which is the main site of lymphocyte differentiation and proliferation, is present in both juveniles and adults. We investigated spleen and bursa mass in relation to parasite measures for 541 Rock Ptarmigan Lagopus muta collected in northeast Iceland during October from 2007 to 2012. Of these 541birds, 540 carried at least one parasite species. Juveniles had heavier spleens than adults, and adult females had heavier spleens than adult males, but there were no sex differences in juveniles. Spleen mass increased from 2007 to 2009, then decreased up to 2011, before slightly increasing again in 2012. Spleen and bursa mass in juveniles increased with improved body condition, but decreased in adults, and this effect differed significantly among years. Spleen mass in juveniles was positively associated with parasite species richness and abundance, in particular endoparasite abundance, with coccidian parasites being the main predictors. Bursa mass was negatively associated with elevated ectoparasite abundance, with two chewing lice being the main predictors. These two immune defense organs appeared to relate to different stimuli. Mean annual spleen mass of juveniles changed in synchrony with Ptarmigan body condition and population density over the years of this study. The only parasite measure that showed any relation to density was coccidian prevalence in juvenile birds, with an approximately 2-year time-lag, suggesting that factors other than parasites are probably more important in triggering changes in spleen mass.
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The relationship between parasites and spleen and bursa mass
in the Icelandic Rock Ptarmigan Lagopus muta
Ute Stenkewitz O
´lafur K. Nielsen
Karl Skı
´rnisson Gunnar Stefa
Received: 12 June 2014 / Revised: 15 September 2014 / Accepted: 11 November 2014 / Published online: 16 December 2014
ÓDt. Ornithologen-Gesellschaft e.V. 2014
Abstract The spleen and bursa of Fabricius in birds are
organs that play an important role in fighting parasite
infections. The size of these organs can be used by ecol-
ogists as a measure of immune investment, with larger size
implying greater investment. The bursa only occurs in
juvenile birds during the development of the B cell reper-
toire, whereas the spleen, which is the main site of lym-
phocyte differentiation and proliferation, is present in both
juveniles and adults. We investigated spleen and bursa
mass in relation to parasite measures for 541 Rock Ptar-
migan Lagopus muta collected in northeast Iceland during
October from 2007 to 2012. Of these 541birds, 540 carried
at least one parasite species. Juveniles had heavier spleens
than adults, and adult females had heavier spleens than
adult males, but there were no sex differences in juveniles.
Spleen mass increased from 2007 to 2009, then decreased
up to 2011, before slightly increasing again in 2012. Spleen
and bursa mass in juveniles increased with improved body
condition, but decreased in adults, and this effect differed
significantly among years. Spleen mass in juveniles was
positively associated with parasite species richness and
abundance, in particular endoparasite abundance, with
coccidian parasites being the main predictors. Bursa mass
was negatively associated with elevated ectoparasite
abundance, with two chewing lice being the main predic-
tors. These two immune defense organs appeared to relate
to different stimuli. Mean annual spleen mass of juveniles
changed in synchrony with Ptarmigan body condition and
population density over the years of this study. The only
parasite measure that showed any relation to density was
coccidian prevalence in juvenile birds, with an approxi-
mately 2-year time-lag, suggesting that factors other than
parasites are probably more important in triggering chan-
ges in spleen mass.
Keywords Bursa of Fabricius Iceland Parasites
Population density Rock Ptarmigan Spleen
Der Zusammenhang zwischen Parasiten und Milz- und
Bursamasse beim isla
¨ndischen Alpenschneehuhn Lag-
opus muta
Die Milz und Bursa Fabricii in Vo
¨geln sind wichtige Org-
ane, die eine Rolle in der Abwehr von Parasiteninfektionen
spielen. Die Gro
¨ße dieser Organe wird von O
gelegentlich als Richtwert von Immuninvestition genutzt,
wobei zunehmende Gro
¨ße mit sta
¨rkerer Investition ver-
bunden wird. Die Bursa existiert nur in Jungvo
¨geln wa
der Entwicklung des B-Zellen Repertoires, aber die Milz,
Communicated by K. C. Klasing.
U. Stenkewitz (&)
Faculty of Life and Environmental Sciences, University of
Iceland, Sturlugata 7, Askja Building, 101 Reykjavı
´k, Iceland
U. Stenkewitz O
´. K. Nielsen
Icelandic Institute of Natural History, Urriðaholtsstræti 6-8,
210 Garðabær, Iceland
U. Stenkewitz K. Skı
Institute for Experimental Pathology, University of Iceland,
Keldur, Keldnavegur 3, 112 Reykjavı
´k, Iceland
G. Stefa
Science Institute, University of Iceland, Dunhaga 5,
107 Reykjavı
´k, Iceland
J Ornithol (2015) 156:429–440
DOI 10.1007/s10336-014-1141-x
welche der Hauptsitz der Lymphozytenabgrenzung und–
vermehrung ist, kommt in Vo
¨geln jeglichen Alters vor. Wir
untersuchten Milz-und Bursamasse im Verha
¨ltnis zu
Parasiten von 541 Alpenschneehu
¨hnern Lagopus muta, die
in Nordost-Island im Oktober von 2007 bis 2012 gesammelt
wurden. Von diesen trugen 540 Vo
¨gel wenigstens eine
Parasitenart. Jungvo
¨gel hatten schwerere Milzen als aus-
gewachsene Vo
¨gel und ausgewachsene Weibchen hatten
schwerere Milzen als ausgewachsene Ma
¨nnchen, aber es
gab keine Geschlechtsunterschiede bei den Jungvo
Milzmassen nahmen von 2007 bis 2009 zu, fielen dann bis
2011, bevor sie in 2012 leicht anstiegen. In Jungvo
nahmen Milz-und Bursamasse mit verbessertem
¨rperzustand zu, aber in ausgewachsenen Vo
¨geln vers-
chlechterte er sich, und dieser Effekt war signifikant u
die Jahre. Milzmasse in Jungvo
¨geln stand in positivem
Zusammenhang mit Parasitenartenfu
¨lle und-ha
¨ufigkeit, be-
sonders Endoparasitenha
¨ufigkeit, wobei Coccidien den
¨ßten Einfluss ausu
¨bten. Bursamasse stand in negativem
Zusammenhang mit erho
¨hter Ektoparasitenha
wobei zwei Kieferlausarten den gro
¨ßten Einfluss hatten. Die
zwei Immunabwehrorgane schienen mit verschiedenen
Stimuli in Zusammenhang zu stehen. Die mittlere ja
Milzmasse von Jungvo
¨geln vera
¨nderte sich synchron mit
dem Ko
¨rperzustand und der Populationsdichte der
¨hner wa
¨hrend den Jahren dieser Untersuchung.
Die einzige Parasiteneinheit, die in Zusammenhang mit der
Populationsdichte stand, war Coccidienprevala
¨nz in Jung-
¨geln, welche den Verlauf mit einer etwa 2-Jahre zeitli-
chen Verzo
¨gerung folgte. Dies gibt zu erkennen, dass
andere Faktoren als Parasiten wahrscheinlich gewichtiger
sind, Vera
¨nderungen in der Milzmasse hervorzurufen.
The spleen and the bursa of Fabricius (hereafter referred to
as ‘‘bursa’’) in birds are immune defense organs that play a
major role in disease resistance (Glick 1956; Cooper et al.
1966; John 1994; Sturkie and Whittow 1999). The bursa is
a primary lymphoid organ in which B lymphocytes are
produced and mature (Sturkie and Whittow 1999; Boehm
et al. 2012), while the spleen is a secondary lymphoid
organ in which lymphocytes are stored and where they
interact with each other and with antigens (John 1994;
Sturkie and Whittow 1999; Powers 2000a). The production
and maintenance of immune organs is considered to be
costly, and birds in good condition should be able to invest
more of their resources in immune function than birds in
poor condition (Sheldon and Verhulst 1996; Derting and
Compton 2003; Schulte-Hostedde and Elsasser 2011).
Infection caused by pathogens can weaken the body
condition of the infected organism and also affect the size
of the immune organs, leading to depletion (atrophy,
hypoplasia, or involution) or enlargement of both the
spleen (splenomegaly) and the bursa (e.g., Glick 1994;
John 1994; Møller et al. 1998a; Powers 2000b; Blanco
et al. 2001). Ecologists have used spleen size as a measure
of the degree of investment in immune defense because its
involvement in fighting systemic disease has frequently
been observed (Powers 2000a). In most studies, high par-
asite abundance in birds has been associated with spleno-
megaly rather than splenic hypoplasia or atrophy (e.g.,
Møller and Erritzøe 1996; Møller et al. 1998a; Powers
2000b; Blanco et al. 2001; Mougeot and Redpath 2004;
Schulte-Hostedde and Elsasser 2011), and increased spleen
size has been positively associated with body condition
(Møller et al. 1998a).
The size of the bursa has been examined less often than
that of the spleen, probably due to its regression prior to
sexual maturity and the need to control statistically any
observed age-related changes. The bursa starts to shrink
before sexual maturity due to the effects of adrenal and sex
hormones, and it is virtually absent in adult birds (Glick
et al. 1956; Sturkie and Whittow 1999; Blanco et al. 2001;
Watson and Moss 2008). Few studies have addressed dif-
ferences in bursa size and body condition due to parasite
infections or the interaction between bursa and spleen size.
However, in their study on House Sparrows Passer do-
mesticus, Møller et al. (1996) reported that birds with large
bursae had more parasites and were in relatively poorer
body condition, whereas birds in good body condition had
smaller bursae. These authors also found that bursa and
spleen sizes were consistently larger in avian species more
prone to parasite infections, such as hole versus open
nesting birds.
There is an age-related decline in immune function
(Ottinger and Lavoie 2007) that is expressed through a
decreased size of immune defense organs, such as the
spleen. This age effect may be related to a variety of fac-
tors, such as immaturity of the immune system of juveniles
(young birds may not yet have encountered the full
diversity of antigens produced by parasites and other
pathogens), trade-off of an investment in immunity for an
investment in growth, or the possibility that immune
responses may be related to changes in structure and size of
the parasite community (Forbes et al. 1999; Hudson et al.
2001; Møller et al. 2003; Hahn and Smith 2011). Invest-
ment in immunity can also be sex dependent, reflecting
dissimilar exposure to parasites, differences in trade-offs
between investment in antiparasite defenses and other
activities related to self-maintenance, survival, and repro-
duction, or to genetic differences in susceptibility (e.g.,
Zuk and McKean 1996; Zuk and Stoehr 2002; Klein 2004;
Møller and Saino 2004; Vicente et al. 2007). There is
430 J Ornithol (2015) 156:429–440
evidence that specific parasite species or groups elicit
specific immune responses rather than responses to the
whole parasite community. For example, in Magpies Pica
pica, ectoparasites are thought to cause a reduction in
spleen mass through their effect on nutritional condition
(Blanco et al. 2001), with nutritional condition reflecting
nutritional status and body condition. Vicente et al. (2007)
associated an increased spleen mass of Red Deer Cervus
elaphus with lungworm Elaphostrongylus cervi infections,
and Cowan et al. (2009) reported that the spleen mass of
Masked Shrews Sorex cinereus increase with bladder
nematode Liniscus maseri infections.
Parasites have been shown to be possible drivers of
population cycles (e.g., Grenfell and Chappell 1995; Bush
et al. 2001). According to the Anderson and May models
(Anderson and May 1979; May and Anderson 1979), this
can happen when (1) parasites show relatively low aggre-
gation within the hosts, (2) parasites impact host fecundity
more than host mortality, and (3) transmission or repro-
duction of parasites shows a time-lag. In Red Grouse
Lagopus lagopus scoticus, for instance, the parasitic nem-
atode Trichostrongylus tenuis increases in response to
grouse density, but with a time-lag, and reduces breeding
success (Hudson et al. 1998). In vertebrates, however,
associations between immune activity and interannual
population changes incorporating pathogens or parasites in
vertebrates have rarely been examined. In studies on
Snowshoe Hare Lepus americanus population cycles, the
parasites lagged hare density by 2–3 years, and hare spleen
weights also changed cyclically, with cycles of spleen
weight preceding the hare population cycle by 1.5 years
(Cary and Keith 1979). However, other studies have not
found correlations between immune organ weights and
population densities (Krebs 1962; Acquarone et al. 2002).
In Iceland, the population cycles of Rock Ptarmigan
Lagopus muta produce peak numbers approximately every
10 years (Nielsen and Pe
´tursson 1995), and parasites could
be one of the triggers.
Based on these aforementioned studies in various avian
species, we hypothesized that bursa and spleen mass in the
Rock Ptarmigan would provide an indication of their
investment in promoting immune responses. We examined
6 years of data and hypothesized that spleen and bursa
mass relate to parasite richness, prevalence, and abundance
of the parasite taxa that are the main targets of immune
responses, and to body condition of the birds. Further, if
parasite infections are important in the case of the Rock
Ptarmigan population cycle, we would expect parasites,
size of immune organs, and body condition to show a time-
lag with respect to Rock Ptarmigan numbers. Birds reach
their best physical condition during the ‘‘increase phase’’ of
the cycle, following which condition declines, reaching
low 2 or 3 years after the peak in numbers and concurrent
with a peak in parasite numbers. This cycle should be more
pronounced for juvenile birds because delayed density-
dependent winter mortality of this cohort is the demo-
graphic driver of the Rock Ptarmigan population cycle in
Iceland (Magnu
´sson et al. 2004).
The area around Lake My
´vatn (65°370N, 17°000W),
northeast Iceland, was the focus of the study. Rock Ptar-
migan (hereafter referred to as Ptarmigan) were collected
in the first week of October for 6 years (2007–2012) on
moorlands, lava fields, and alpine areas west, east, and
north of the lake. The birds were collected by gunshot
outside the hunting season under a license issued by the
Icelandic Institute of Natural History (IINH).
The first week of October was chosen as our reference
point to (1) control for seasonal changes in spleen and
bursa size, as well as parasite measures (e.g., John 1994;
´ttir et al. 2010; Akbar et al. 2012), and (2)
sample the Ptarmigan population at the onset of winter
because winter survival determines population change
(Garðarsson 1988). Ptarmigan are free-flying wild birds;
consequently, individuals could not be selected at random,
but were collected by conventional walk-up hunting. The
birds were shot sitting or flying when encountered in areas
where they gather during this season. In each year, there
was a surplus number of juvenile birds in the catch, and
individuals in this group were selected at random for
A total of 541 Ptarmigan (179 juvenile males, 177
juvenile females, 122 adult males, 63 adult females) were
analyzed. Each bird was tagged immediately after collec-
tion, wrapped in absorbent paper, placed in a paper bag,
cooled to 4 °C, and transported to the laboratory at the end
of the day. All birds were dissected within 3 days of col-
lection. Birds were sexed using both the loral stripe and the
size and color of the combs (Montgomerie and Holder
2008), and age was based on pigmentation of the primaries
(Weeden and Watson 1967). Sex and age were confirmed
during necropsy by inspection of the gonads and presence
or absence of the bursa. Two age classes were recognized:
juveniles (about 3 months old) and adults (about
15 months or older). Ptarmigan become mature as 1 year
olds (Holder and Montgomerie 1993). Mortality rates in the
Icelandic Ptarmigan population are high, and few birds
exceed the age of 4 years (Garðarsson 1988; IINH ringing
To obtain an index of body condition, we took the fol-
lowing external and internal morphometric measurements
for each bird: (1) wing length, measured to the nearest
millimeter with a ruler from the carpal joint to the tip of the
J Ornithol (2015) 156:429–440 431
flattened and straightened wing, (2) head ?bill length,
measured to the nearest 0.1 mm with calipers from the
hindmost point of the head to the tip of the bill, (3) tarsus
length, measured to the nearest 0.1 mm with calipers from
the joint between tarsus and mid-toe to the intertarsal joint,
(4) tarsus ?mid-toe length, measured to the nearest mil-
limeter with a ruler from the ‘‘heel’’ to the base of the
central claw, (5) sternum length, measured to the nearest
millimeter with calipers from the tip of the Spina externa
along the center line to the Margo caudalis, and (6) ster-
num–coracoid length, measured to the nearest 0.1 mm with
calipers from the center line of the Margo caudalis to the
cranial end of the Coracoideum. Anatomical terms are
according to Baumel (1979). The six body measures [(1)–
(6)] were highly correlated with each other. A principle
component analysis (PCA) was used to derive an index of
structural size using Factor 1 from the PCA. Factor 1
explained 61.4 % of the variance in the original variables
and was highly related to them (loadings: wing =0.831,
head ?bill =0.833, tarsus =0.528, tarsus ?mid-
toe =0.647, sternum =0.891, sternum-cora-
coid =0.899). To obtain the index of body condition, body
mass was regressed on body size, and the residuals used as
a body condition index.
The spleen is located in the abdomen and is situated
dorsally at the angle between the proventriculus, the giz-
zard, and the liver (Powers 2000a). In Ptarmigan, it is tri-
angular and pink to red-brown. The bursa is a pink pouch
connected dorsally to the cloaca and opening into it
(Sturkie and Whittow 1999). The spleen and the bursa were
removed during necropsy and weighed on a digital scale
(accuracy 0.0001 g).
´rnisson et al. (2012) provide a detailed description of
collection and quantification methods for ectoparasites and
endoparasites (Table 1). Quantification of the mite species
Tetraolichus lagopi,Metamicrolichus islandicus, and
Mironovia lagopi was adapted. Scores and direct counts
from vacuum filters were combined for total scores. For the
feather mite T. lagopi, abundance was scored by viewing
the underwing coverts of the primary flight feathers and
alula feathers against a strong light source. Single mites
were seen as reddish dots close to the shaft of the white
feathers, but mites also occurred in clumps. Scores from 0
to 3 were used to describe abundance, where 0 =no mites
present, 1 =few or some dozens of mites present, seen as
isolated reddish dots, 2 =narrow, reddish mite accumu-
lations seen on some affected feathers, and 3 =broad (up
to 2–3 mm wide) accumulations of mites seen on infested
feathers. Both filter count and score data were cross
checked to confirm infestation. If mites were present in the
filter, but not observed during scoring, that bird was given a
score of 1. Hence, a score of 1 indicated both minor
infestation with this mite species and its presence. For the
prostigmatan mite M. lagopi living in feather shafts on the
wing, seven feathers from the middle of the wing (two
upper-wing greater primary coverts and five secondary
flight feathers) were examined. Each feather was scored,
where 0 =no mites present; 1 = B10 mites present, and 2
=[10 mites present. The scores were added to derive a
value for each individual. Ptarmigan were also scored for
mange. Mange is a skin disease caused by skin mites—in
the case of Ptarmigan, M. islandicus. Infested skin appears
dry and scaly. Feathers from the chest, sides, and back of
each bird were plucked, and scores of 0–3 were used to
describe mange extent, with 0 =no scales, 1 = \25 % of
the body covered with scales, 2 =25–75 % of skin with
scales, and 3 = [75 % of skin with scales. Both count and
score data were cross checked to confirm infestation of the
bird. If mites were present in the filter, but not observed
during scoring, that bird was given a score of 1. Hence, a
score of 1 indicated both minor scaly skin and the presence
of skin mites.
Each spring, territorial male Ptarmigan were counted on
six plots in the study area. The total size of these plots was
26.8 (range 2.4–8.0) km
. Each plot was censused once
during May (range 10–24 May). This census was con-
ducted on foot by at least two observers in the early
morning (0500–1000 hours) or late afternoon (1700–2400
hours). The positions of territorial males as well as the
locations of Ptarmigan kills were plotted on a map. A
‘kill’’ indicated the remains of a Ptarmigan killed and
eaten after arrival on the census plot in the spring. The total
number of males counted in the spring census was the sum
of the number of territorial males censused and those
killed. The Ptarmigan index used for this study was the
annual mean density of males on these six plots. Nielsen
(1996) provides a detailed description of the census plots
and methods.
Statistical analyses
Statistical analyses were done using the software package
R Core Team 2011; ver. 2.14.1). All tests were two-tailed,
and differences were deemed significant at P\0.05. The
frequency distributions of spleen and bursa mass were
assessed using a Shapiro–Wilk test. Spleen mass was right
skewed and thus log transformed to ensure normal distri-
bution of the data. Year was treated as a factor (i.e., cate-
gorical variable). The parasite data for each species were
ranked in ascending order (1 was allotted to the lowest
positive finding) and midranks were used to account for
ties (Holmstad et al. 2005). The ranked values of each
parasite species were then summed to derive the total
parasite, ectoparasite, and endoparasite abundance for each
individual host and so enable the different counting units of
the parasite groups to be combined. For the parasite groups
432 J Ornithol (2015) 156:429–440
‘coccidians,’’ ‘‘helminths,’’ and ‘‘lice,’’ the original para-
site count data of the respective parasite species were
summed for each individual host. Parasite richness was
defined as the total number of parasite species living in or
on the host (Margolis et al. 1982; Bush et al. 1997; Schulte-
Hostedde and Elsasser 2011). Parasite prevalence was
defined as the proportion of hosts infected by a particular
parasite species (Bush et al. 1997; Schulte-Hostedde and
Elsasser 2011). Mean parasite abundance (hereafter refer-
red to as parasite abundance) was defined as the sum of
individuals of a particular parasite species in a sample of
hosts divided by the number of hosts examined (Bush et al.
1997). Parasite count data of Amyrsidea lagopi and Cera-
tophyllus garei for adult birds and C. garei for juvenile
birds were not used in further analyses due to small sample
sizes. Helminths were analyzed as a group due to small
sample sizes of the different species.
Linear models were used to test whether spleen and
bursa mass were related to body size, age, sex, year and
body condition index and to investigate interactions
between these variables. The stepwise backwards proce-
dure was adopted, i.e., the least important variables
(highest Pvalues) were removed from the model until only
the significant (PB0.05) variables remained. Following
this analysis, parasite measures and individual parasite
species or groups, each tested separately, were added to the
model, and it was reanalyzed controlling for the significant
variables in the preceding model. Alpha levels (P\0.05)
were adjusted using Holm–Bonferroni corrections. Linear
models were used to test whether spleen mass was asso-
ciated with bursa mass, controlling for body size and
Ptarmigan population density.
Of the 541 Ptarmigan analyzed, 540 had at least one par-
asite species, with 540 carrying ectoparasites and 449
carrying endoparasites. The parasites included four species
of astigmatan feather mites and one prostigmatan quill mite
(Acari), two ischnocerid and one amblycerid chewing lice
(Mallophaga), two coccidians (Sporozoa), three helminths
(two Nematoda and one Cestoda), one fly (Diptera), and
one flea (Siphonaptera; Table 1). All parasite species were
more abundant in juvenile birds, with the exception of the
nematodes Capillaria caudinflata and Trichostrongylus
tenuis, which were more abundant in adult birds (Table 1).
Most prevalent was the mite Tetraolichus lagopi, followed
by the coccidian Eimeria muta and the louse Goniodes
lagopi (Table 1).
Table 1 The ecto- and endoparasite fauna of Rock Ptarmigan (Lagopus muta) in northeast Iceland during each October 2007–2012
Parasite group Scientific name Number of infected hosts
Prevalence all
Prevalence juveniles
Prevalence adults
Acari (mites) Metamicrolichus islandicus 29.1 31.9 21.6
Myialges borealis 14.4 18.6 5.3
Mironovia lagopus 5.9 2.8 12.3
Strelkoviacarus holoaspis 42.5 55.0 27.8
Tetraolichus lagopi 99.2 100.0 98.3
Chewing lice (lice) Amyrsidea lagopi 13.1 18.5 2.7
Goniodes lagopi 71.8 84.0 48.1
Lagopoecus affinis 51.2 64.2 25.4
Diptera (flies) Ornithomya chloropus 37.3 39.4 35.7
Siphonaptera (fleas) Ceratophyllus garei 0.4 0.6 0.0
Sporozoa (coccidians) Eimeria muta 75.4 77.5 71.7
Eimeria rjupa 12.8 13.4 11.5
Cestoda (tapeworms) Passerilepis serpentulus 1.2 1.1 0.0
Nematoda (roundworms) Capillaria caudinflata 28.4 27.5 32.5
Trichostrongylus tenuis 2.7 2.3 2.9
Blastocystis sp. was present, but not quantified
J Ornithol (2015) 156:429–440 433
Spleen and bursa mass
Spleen mass ranged from 0.024 to 0.243 g and was not
significantly related to body size (F
P=0.840; Table 2). Variation in spleen mass was due to
age and year (age: F
=62.80, P\0.001; year:
=2.57, P=0.026), as well as to the interaction of
age and body condition (F
=11.77, P\0.001).
Consequently, juveniles had heavier spleens than adults,
and mean spleen mass increased from 2007 to 2009, then
decreased to 2011, before slightly increasing again in 2012
(Table 2; Fig. 3). While spleen mass increased in juveniles
with increasing body condition, it decreased in adults
(Fig. 1).
Variation in spleen mass of juvenile birds was due to
body condition (F
=12.10, P\0.001), as well as to
the interaction of body condition and years (F
P=0.042). Accordingly, spleen mass increased with
improved body condition (Fig. 1), but the effect of body
condition differed among years. While with improved
condition, spleen mass increased in almost all years, it
decreased in 2009 and decreased slightly in 2012. There
was no significant variation in spleen mass among the
sexes (F
=1.60, P=0.207; Table 2).
Variation in the spleen mass of adult birds was mar-
ginally due to sex (F
=3.81, P=0.053), as well as to
the interaction of body condition and years (F
P=0.027). As such, adult females tended to have heavier
spleens than males (Table 2), and the effect of body con-
dition differed between years. While spleen mass decreased
in almost all years with improved body condition, it
increased in 2009 and 2012.
Bursa mass ranged between 0.059 and 0.466 g and was
significantly positively related to body size (F
P\0.030; Fig. 1). Variation in bursa mass was due to
body condition (F
=20.02, P\0.001; Table 2)as
well as the interaction of body condition and year
=5.23, P\0.001). Therefore, bursa mass
increased with improved body condition in all years, but
the slopes differed between years. There was no significant
variation in bursa mass among the sexes (F
P=0.471; Table 2).
Spleen and bursa mass in relation to parasite measures
Spleen mass in juvenile birds increased significantly with
increasing parasite species richness (Fig. 2) and abun-
dance; this was particularly true for endoparasite abun-
dance and the abundance of the skin mite M. islandicus
(Table 3). Regarding parasite prevalence, spleen mass was
significantly greater when coccidians and the skin mite M.
islandicus were present (Table 3). Spleen mass in adult
birds had no significant relationship with parasite measures
(Table 3).
Bursae were significantly lighter when ectoparasites
were more abundant, and particularly when the chewing
lice Lagopoecus affinis and G. lagopi were present
(Table 3).
Table 2 Mean spleen and bursa
mass of Rock Ptarmigan
(Lagopus muta) in northeast
Iceland during each October
Data are presented as the
mean ±standard deviation
Organ Age Sex Year Sample size (N) Mean mass (g)
Range (g)
Spleen Juvenile Both 2007 60 0.070 ±0.019 0.035–0.110
2008 57 0.076 ±0.026 0.036–0.162
2009 59 0.084 ±0.031 0.039–0.243
2010 60 0.076 ±0.030 0.030–0.197
2011 60 0.067 ±0.019 0.031–0.119
2012 60 0.071 ±0.025 0.026–0.172
Female All 177 0.075 ±0.027 0.026–0.243
Male All 179 0.073 ±0.024 0.024–0.197
Adult Both 2007 20 0.052 ±0.020 0.029–0.114
2008 25 0.057 ±0.019 0.034–0.107
2009 19 0.084 ±0.031 0.024–0.113
2010 40 0.056 ±0.020 0.027–0.102
2011 41 0.060 ±0.022 0.026–0.111
2012 40 0.058 ±0.019 0.033–0.113
Female All 63 0.063 ±0.023 0.024–0.114
Male All 122 0.056 ±0.019 0.027–0.113
Bursa Juvenile Female All 174 0.231 ±0.070 0.059–0.412
Male All 178 0.262 ±0.076 0.101–0.466
434 J Ornithol (2015) 156:429–440
Spleen versus bursa mass
Spleen and bursa mass, corrected for body size, were not
related (F
=0.65, P=0.420).
Spleen and bursa mass in relation to Ptarmigan density
Spleen mass (F
=5.57, P=0.019), but not bursa
mass (F
=0.03, P=0.872), was significantly posi-
tively related with Ptarmigan density (Fig. 3; Table 4). The
2009 autumn peak in spleen mass and body condition was
succeeded by a peak in Ptarmigan density in spring 2010.
i.e., spleen mass tracked population change synchronously
(Fig. 3).
In juvenile Ptarmigan, we found that spleen mass was
positively associated with parasite species richness and
parasite abundance and was particularly positively associ-
ated with endoparasite abundance, the presence of cocci-
dians, and the mite M. islandicus. Bursa mass was
negatively associated with ectoparasite abundance, in par-
ticular with the presence of chewing lice (Table 3). In other
words, spleen mass increased and bursa mass decreased
with increased parasite abundance, but changes in the two
organs were associated with different parasite groups, and
masses were not significantly correlated. Most studies have
reported an increase in size of the spleen (splenomegaly:
see John 1994; Møller and Erritzøe 1996; Sturkie and
Whittow 1999; Møller et al. 1998a; Morand and Poulin
2000; Powers 2000a) and bursa (e.g., Glick 1994; Møller
and Erritzøe 1996; Møller et al. 1996) if parasites instigate
an immune response, but a few studies do observe or
suggest spleen size decrease with an increase in parasites
(e.g., Møller et al. 1998b; Shutler et al. 1999; Vicente et al.
2007). We are unaware of other studies reporting reduced
bursa mass associated with increased parasites.
Spleen, bursa, and parasite measures: age, body
condition, sex, and year effects
Splenomegaly in juvenile Ptarmigan was significantly
positively associated with parasite richness and abundance,
with lighter bursae associated with ectoparasite abundance.
Fig. 1 Effect of body condition on spleen mass (log-transformed) in juvenile (left) and adult (middle) Rock Ptarmigan (Lagopus muta), as well
as bursa mass in juvenile (right) Rock Ptarmigan in northeast Iceland each October between 2007 and 2012. Lines linear regression lines
Fig. 2 Associations between
spleen (log-transformed) mass
and parasite richness and
abundance of juvenile Rock
Ptarmigan (Lagopus muta)in
northeast Iceland each October
between 2007 and 2012. Line
linear regression line
J Ornithol (2015) 156:429–440 435
In contrast, adult Ptarmigan did not show any relation
between spleen mass and parasite richness and abundance.
Furthermore, the spleen and bursa mass of juvenile birds
was positively related to body condition, while the spleen
mass of adults was negatively related to body condition
(Fig. 1). Møller et al. (1998a) found larger spleens in birds
of good body condition but also in diseased individuals.
These authors concluded that spleen size responds more
strongly to changes in body condition than to changes in
disease status. They also showed a strong correlation
between condition and immune function, suggesting that
the main cause of a weak immune response is poor body
condition. In our study, the age-related difference in
investment in immune function suggests that young birds
are more susceptible to parasites and that they need to
invest more in immune defense than adult birds. Hence,
according to Møller et al. (1998a), the prerequisite of a
strong immune response in juvenile birds should be good
body condition (Fig. 1). This is similar to findings for
Magpies, where first-year birds were found to be more
Table 3 Association between
mass of bursa and spleen (log-
transformed) and parasite
species richness, parasite
abundance, and prevalence of
Rock Ptarmigan in northeast
Iceland during each October
* Significant at P\0.05 after
Holm–Bonferroni correction
The linear models were
corrected for year, sex, body
size, or body condition index.
Ranked data were used for total
parasite, endoparasite, and
ectoparasite abundance.
Analyses for T. lagopi
prevalence were omitted as
these Acari were present on at
least 98.3 % of the birds. For
other omitted values, the sample
size was too low
Factors Bursa juvenile
(df =349)
Spleen juvenile
(df = 348)
Spleen adult
(df =182)
tP tP tP
Parasite richness -1.58 0.116 2.81 0.035* 0.66 0.513
Parasite abundance -1.66 0.098 2.63 0.036* 0.54 0.594
Endoparasite abundance 0.35 0.177 3.24 0.010* 0.55 0.584
Coccidians 0.28 0.783 1.23 0.221 -0.04 0.967
Eimeria muta -1.16 0.249 1.39 0.167 -0.03 0.976
Eimeria rjupa 1.29 0.200 0.44 0.658 -0.14 0.888
Helminths 0.17 0.869 0.76 0.450 0.23 0.822
Ectoparasite abundance -2.76 0.036* 1.13 0.261 0.24 0.814
Metamicrolichus islandicus -1.93 0.066 2.52 0.036* 0.11 0.912
Myialges borealis -0.61 0.545 1.44 0.150 1.21 0.230
Strelkoviacarus holoaspis 0.93 0.354 0.71 0.477 -0.94 0.351
Tetraolichus lagopi -2.13 0.034 0.21 0.831 -0.22 0.830
Mironovia lagopi -1.63 0.104 -0.88 0.379 1.08 0.280
Chewing lice -1.50 0.135 -0.96 0.339 1.26 0.210
Goniodes lagopi -2.15 0.066 -0.39 0.696 0.57 0.569
Lagopoecus affinis -1.40 0.161 -1.75 0.082 1.92 0.056
Amyrsidea lagopi 1.15 0.252 -0.12 0.907
Ornithomya chloropus 1.72 0.087 -0.39 0.697 0.46 0.648
Parasite presence/absence
Coccidians -0.32 0.752 4.28 \0.001* 0.74 0.460
E. muta -0.91 0.365 4.19 \0.001* 0.21 0.833
E. rjupa 0.72 0.474 3.13 \0.001* 1.59 0.114
Helminths 1.63 0.104 -0.13 0.901 -0.58 0.565
M. islandicus -1.31 0.190 2.79 0.036 -0.70 0.487
M. borealis -0.91 0.364 1.66 0.098 0.39 0.698
S. holoaspis 0.13 0.894 0.23 0.822 0.03 0.980
M. lagopi -1.24 0. 216 -0.94 0.347 1.01 0.314
Chewing lice -3.32 \0.001* -0.81 0.419 1.40 0.165
G. lagopi -2.95 0.024* -0.78 0.435 0.94 0.349
L. affinis -3.25 0.010* -0.92 0.359 0.93 0.355
A. lagopi 0.31 0.758 0.27 0.790
O. chloropus 0.74 0.462 0.09 0.926 -0.74 0.462
436 J Ornithol (2015) 156:429–440
parasitized than adults and where spleen size increased
with the condition of the birds (Blanco et al. 2001), just like
in juvenile Ptarmigan. The adult Ptarmigans in our study,
however, had fewer parasites, possibly because they
acquired immunity over time or because differences in
mortality rates may have eliminated susceptible individuals
from the population, leaving predominantly resistant
adults. Our findings suggest that adults in bad condition
invest more in immune function than adults in good con-
dition (Fig. 1).
Adult female Ptarmigans carried more parasites than
their male counterparts and, accordingly, the spleen mass
of adult females was generally greater than that of adult
males. This may reflect differences in sex roles. We col-
lected our birds during the first week of October, approx-
imately 5 weeks after brood break-up (Holder and
Montgomerie 1993; Watson and Moss 2008). The female
cares for the chicks alone. This is an energy-demanding
activity, and brooding should expose adult females to
parasites much more than males because the growing
chicks become a hot spot for parasites. This effect may be
further enhanced when broods mix in late summer.
Accordingly, females should invest more in immune
defense than males, resulting in greater spleen mass.
Similarly, in a variety of bird species, Møller et al. (1998b)
found that sex differences in spleen and bursa size were not
present among juveniles, but that adult males had consis-
tently smaller spleens than adult females. These authors
suggested that sex differences in immune function may
evoke sex differences in parasitism, but reasoned that adult
females with larger immune defense organs would be
healthier and less prone to parasite infections than males.
This is contrary to our findings for the Ptarmigan. How-
ever, in the same study, Møller et al. (1998b) also showed
that females have initially larger immune organs than
males due, for example, to the suppressive effects of
androgens in males. Therefore, we cannot rule out that sex
differences in spleen mass are solely due to sex
Spleen, bursa, and parasites: effect of particular parasite
Different parasite groups together with increased body
condition were related to different spleen and bursa mass
effects in juvenile birds. For example, juveniles seemed to
be particularly prone to coccidian infections, and their
spleens were heavier when coccidians were present. These
parasites can cause coccidiosis (Powers 2000b) that could
stimulate an immune reaction leading to splenomegaly.
Coccidian infections occur frequently because juvenile
birds have not yet acquired the mature immune function
found in adult birds. The annual peaks in coccidian
intensity and prevalence for both juvenile and adult birds
occur in October, the month Ptarmigan were collected
during our 6-year study (Þo
´ttir et al. 2010). The
prevalence and abundance of skin parasites were associated
with increased spleen mass. Ectoparasites have been found
to be associated with splenomegaly and increased immune
function (Blanco et al. 2001; Brown and Brown 2002). M.
islandicus live in the upper skin layer and feed on the
epidermal tissue and body fluids of the Ptarmigan. This
mite causes mange in Ptarmigan and should therefore
provoke immune responses.
Bursae were lighter when the lice Lagopoecus affinis
and Goniodes lagopi were present and G. lagopi abundant,
but the relationship was negative. Both these ischnoceran
chewing lice feed primarily on feathers and dead skin,
whereas the more mobile amblyceran Amyrsidea lagopi
feed on living tissue, such as skin and blood (Price et al.
2003; Clayton et al. 2008). It is hard to conceive that the
presence of these ischnoceran chewing lice should elicit an
immune response. The relationships we observed could
thus be coincidental because A. lagopi did not relate to
Fig. 3 Annual variation in spleen mass (log-transformed; solid black
line), body condition (dashed black line), and prevalence of
coccidians (solid grey line) in juvenile Rock Ptarmigan (Lagopus
muta), and Rock Ptarmigan population density (dotted black line)in
northeast Iceland. Spleen, parasite, and body condition data were
obtained each October 2007–2012. Ptarmigan density numbers were
obtained each May 2007–2013. Values are standardized to (x-l)/s
Table 4 Mean densities of
Rock Ptarmigan (Lagopus muta)
on six census plots in northeast
Iceland during each May
Year Mean
2007 4.03 0.992
2008 5.58 1.247
2009 7.35 1.362
2010 7.93 1.373
2011 4.28 0.864
2012 3.53 0.698
2013 4.00 0.749
J Ornithol (2015) 156:429–440 437
variation in bursa mass. In their study on ischnoceran and
amblyceran chewing lice and the immune response of
avian hosts, Møller and Rosza (2004) found no relationship
between host immune response and ischnoceran chewing
lice, contrary to that found for amblycerans. Other agents,
such as bacteria, fungi, or viruses, may be more important
factors driving changes in bursa mass. There should in
particular be more efficient defenses against lice, such as
preening behavior and the use of preen oil from the preen
gland (Moyer et al. 2003; Clayton et al. 2010).
Spleen mass: the year effect and Ptarmigan density
The spleen mass of juvenile birds varied among years in a
cyclic pattern, being low at the start of the study in 2007,
increasing to a peak in 2009, and then declining to a
minimum in 2011, before increasing again in 2012 (Fig. 2).
Adult spleen mass showed the same general annual pattern,
albeit not as significantly.
Mean spleen mass of juvenile birds in the autumn was
positively correlated with body condition and Ptarmigan
density the following spring (Fig. 3). Mean bursa mass was
only correlated with body condition, but not density. These
results suggest that juvenile Ptarmigan with large spleens
and bursae have a good body condition and are therefore in
line with those of other studies (e.g., Møller et al. 1998a;
Vicente et al. 2007; Schulte-Hostedde and Elsasser 2011).
One parasite group, however, did show an annual pattern
similar to that observed for spleen mass, body condition,
and Ptarmigan population density—but with a time-lag;
this was the coccidians in juvenile birds (Fig. 3). We
hypothesized that if parasite infections are important in the
Ptarmigan population cycle, we would expect parasites,
immune organ size, and body condition to show a time-lag
with respect to Ptarmigan numbers. Prime condition should
be reached during the ‘‘increase phase’’ of the Ptarmigan
cycle, following which it should decline to a low around 2
or 3 years after the peak in Ptarmigan numbers, concurrent
with a peak in parasite numbers. Also, this cycle should be
more pronounced for juvenile birds. However, the mis-
match in the annual pattern among coccidian prevalence as
well as spleen mass and body condition is contrary to our
hypothesis and suggests that other factors may be more
important in triggering immune function in the Ptarmigan.
Møller et al. (1998a) proposed that hypersensitivity reac-
tions could be one alternative explanation for finding large
immune defense organs in diseased birds.
Spleen mass in our collected Rock Ptarmigan was posi-
tively associated with parasite species richness and
abundance, in particular with endoparasite abundance,
presence of coccidians, and a mange-inducing mite—but
only in juveniles. Bursa mass was negatively associated
with ectoparasite abundance—in particular with the pre-
sence of certain chewing lice. The two immune defense
organs together with the body condition of the birds were
associated with the abundance and prevalence of different
parasite groups and species, and changes in size of the
organs were not correlated. Changes in the spleen mass of
juvenile Ptarmigan over the years of the study were
approximately synchronous with changes in body condition
and population density, but coccidian prevalence lagged
behind population change by approximately 2 years.
Hence, we conclude that the parasites investigated in our
study are not the only trigger for changes in spleen and
bursa mass in juvenile Ptarmigan and that other factors are
possibly more important. There is evidence that micro-
parasites such as bacteria and viruses inflict stronger
immune responses. Our study showed that spleen mass was
a marker of immune response in the Ptarmigan; however,
there may be more suitable tools for monitoring immune
investment in response to parasite burden, such as immu-
nogenetics. Even so, spleen mass is more suitable than
bursa mass because spleen mass is independent of body
size, both age groups have spleens, and the spleen shows a
significant positive relationship with certain parasite
Acknowledgments This project was financially supported by the
Icelandic Research Fund (Grant Number 090207021), Icelandic
Hunter’s Fund, Landsvirkjun Energy Fund, Institute of Experimental
Pathology (KELDUR) at University of Iceland, and Icelandic Institute
of Natural History. Logistical help was provided by the Icelandic
Institute of Natural History, My
´vatn Research Station, and Northeast
Iceland Nature Center. For help in the field and the laboratory we
thank S.S. A
´rnason, M. le Barh, A. Bjarnasson, Þ.Þ. Bjo
¨rnsson, I.
Blazquez de Paz, M. Donofrio, P.C. Garcia Galindo, J. Geiger, A.F.
Guðmundsson, G.A. Guðmundsson, G. Halldo
´rsson, H. Haraldsson,
M. Holzapfel, E. Igersheim, F.L. Jo
´hannsson, F. Jo
´nasson, F. Karls-
son, D. Lange, V. Mader, K.P. Magnu
´sson, K. Pelletier, N. de Pels-
maeker, K. Ries, A. Schlaich, I. Schwenkmeier, O
´.G. Sigurðardo
¨. Snæþo
´rsson, H.W. Stefa
´nsson, S. Thirgood, D. Zeugler, S.Þ.
´ttir, Þ.L. Þo
´rarinsson, and V. Moos. We thank S.
´ttir, A.P. Møller, and two anonymous reviewers for their
valuable comments on this manuscript, and A. Galkin, A.V. Bochkov,
R.L. Palma, R.E. Lewis, R. Stensvold, S.V. Mironov for describing or
confirming identifications of parasites. This study complies with the
current laws of Iceland.
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Nat 160[Suppl 4]:S9–S22
440 J Ornithol (2015) 156:429–440
... The hen therefore broods the chicks for the first month of their lives, and this social interaction affords the opportunity for vertical transmission of ectoparasites (Skírnisson and Nielsen 2019). Transmission of ectoparasites to and from hens could be further heightened by the energetic costs of brood rearing (Stenkewitz et al. 2015). The males do not take part in caring for the brood. ...
... For example, Stenkewitz et al. (2015) showed that adult females had greater spleen masses than males, suggesting that females invest more in immune defense in our study population. However, adult females were still acquiring more parasites of several species than males, compared to other related host species (above). ...
... However, adult females were still acquiring more parasites of several species than males, compared to other related host species (above). The authors believe that the energetic task of brooding and rearing offspring (female-only tasks) may have made them more susceptible to infection during that time of year (Stenkewitz et al. 2015). This is especially the case for directly-transmitted parasites such as coccidians, lice and mites, which are more likely to accumulate in birds that were more group-living before being sampled (juveniles and adult females) compared to those that were more solitary (adult males). ...
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.
... Infestation of the three mallopagan species and ptarmigan body condition are not significantly associated (Stenkewitz et al. unpubl.). There is though a negative relationship between preen gland mass and prevalence of all three mallophagan species (González 2014), and also between the mass of the bursa of Fabricius -an organ of immune function in young birds -and the prevalence of G. lagopi and L. affinis (Stenkewitz et al. 2015). Both of these observations imply that there are physiological costs associated with mallophagan infestations in ptarmigan. ...
... 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. ...
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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.
... The high and stable nest temperature is also favored by nest parasites (fleas, lice and ticks) and their abundances increase with a more stable microclimate (Sinclair and Chown 2006). Nest parasites have a substantial negative effect on the incubating bird due to blood loss and increased possibility of infections (Möller 1993, Oppliger et al. 1994, Bush et al. 2001, Lesna et al. 2009, Clayton et al. 2010, Mainwaring et al. 2014, Stenkewitz et al. 2015, Wetherbee 2016). ...
... However, such high and stable nest temperatures during incubation, maintained by high incubation constancy, also favour nest-living ectoparasites (fleas, lice and ticks), as abundances of ectoparasites in the nests have been observed to increase in a favourable thermal microclimate (Sinclair & Chown 2006). Accumulating evidence shows that ectoparasites have substantial negative effects on incubating birds due to loss of blood and increased probabilities of infections (Möller 1993, Oppliger et al. 1994, Bush et al. 2001, Lesna et al. 2009, Clayton et al. 2010, Mainwaring et al. 2014, Stenkewitz et al. 2015. Breiðafjörður, West Iceland, is an important breeding, moulting and wintering area for Eiders and supports at least 20-25% of the Icelandic Eider population , which is estimated about 850 000 birds in winter ). ...
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Breiðafjörður Bay, West Iceland, is an important breeding, molting and wintering area for the Common Eider (Somateria mollissima) (hereafter Eider). Eider farmers have collected nest down for centuries in the area. The aims of the doctoral thesis centered on feeding and breeding ecology of Eiders in Breiðafjörður. The incubation behavior in a very dense colony (Rif, 1.7 nests/m2) was studied to evaluate whether the incubating females helped each other through the incubation by attending more than one nest. Incubation cost was indexed with mass loss of the females during the incubation period and was compared between nests with and without down removal, and between females with enlarged clutches (≥7 eggs) and those incubating normal clutches (≤6 egg). Ectoparasites were collected from the Eider nests and abundances of the flea (Cerotophyllus garei) was compared between two colonies at Rif and Hvallátur. The spring/early summer (May-July) diet of the Eiders was investigated between years, months and sexes. Cooperative incubation behavior was confirmed with marked Eiders in the superdense colony at Rif. The females attended each other‘s nests, which may be a behavioral response to lack of new nesting sites and visual stimulus as they see many unguarded nests close to their own. Eiders at Rif might own some eggs in more than one nest in the colony. The ectoparasitic load at Rif is very high and the cooperative behavior gives the incubating females more time to leave their nests to preen while other Eiders attend their nests. At the more sparsely-nested colony at Hvallátur cooperative incubation has never been observed but there Eiders can switch nesting bowls between years if ectoparasitic loads become high. The key food item in spring/early summer feeding was the mottled red chiton (Tonicella marmorea). Chitons have not been considered an important food item for Eiders until now. Down collection was not found to have effect on the incubating Eiders, during these average weather conditions. Likewise, the enlarged clutches did not affect energy expenditure of incubating females or their hatching success. Down collection can therefore be considered to be environment-friendly as it does not harm the incubating Eiders.
... The ectoparasites included skin mites Metamicrolichus islandicus (known to cause mange) and Myialges borealis, the two often appearing in co-infections (Stenkewitz et al., 2015). The quill mite (Mironovia lagopus), another ectoparasite, was infrequently sampled, whereas the two remaining mite species Strelkoviacarus holoapsis and the wing mite Tetraolichus lagopi were often sampled on birds (T. ...
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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.
... One of the major roles of the spleen is to produce and store lymphocytes that function in antibody-and cell-mediated immunity, and this organ can increase in size during infections (reviewed in : John, 1994;Smith and Hunt, 2004). With respect to parasitic infections specifically, the spleen is thought to play an integral role in the immune response, and several studies have shown that spleen mass is higher in individuals with higher parasite loads (e.g., Figuerola et al., 2005;Robinson et al., 2008;Stenkewitz et al., 2014). However, this is not always the case and a negative (Shutler et al., 1999) or no relationship (Mallory et al., 2007) have also been reported. ...
Daily energy expenditure (DEE) in animals is influenced by many factors although the impact of stressors remains largely unknown. The objective of this study was to determine how multiple physiological stressors (parasite infection and contaminant exposure) and natural challenges (energy-demanding activities and weather conditions) may affect DEE in nesting ring-billed gulls (Larus delawarensis) exposed to high concentrations of persistent organic contaminants (POPs). Physical activity, temperature, gastrointestinal parasitic worm abundance, relative spleen mass, plasma thyroid hormone levels and liver concentrations of POPs were determined; field metabolic rate (FMR) was used as a measure of DEE. For females, FMR was best explained by the percent of time spent in nest-site attendance and exposure to temperatures below their lower critical limit (65% of variation); 32% was also explained by relative spleen mass. In males, FMR was best explained by the number of hours spent in nest site attendance and either relative spleen mass or liver concentrations of tetra-brominated diphenyl ethers (tetra-BDEs) (55% of variation). Relative spleen mass, as an important factor relating to FMR, was best explained by models with a combination of parasite abundance (Diplostomum for females and Eucoleus for males) in a negative relationship, and liver POP concentrations (p,p’-DDE for females and tetra-BDEs for males) in a positive relationship (34%, 55% of variation for females and males, respectively). This study demonstrates that immune activity may be an important factor affecting energy expenditure in ring-billed gulls, and that contaminants and parasite abundance may have both a direct and/or indirect influence on FMR.
... The data suggest that juveniles suffer more from C. caudinflata infections than adults, i.e. the relationship with the mortality rates; C. caudinflata infections seem to be one of the drivers of the Z X,W rate (mortality in August through April). That juveniles suffer more from C. caudinflata infections than adults may have to do with varying levels of immune function to resist or treat infections [66]. The reverse relation between fecundity and the amblyceran chewing louse Amyrsidea lagopi prevalence is of interest (Fig 6). ...
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Populations of rock ptarmigan (Lagopus muta) in Iceland fluctuate in multiannual cycles with peak numbers c. every 10 years. We studied the ptarmigan-parasite community and how parasites relate to ptarmigan age, body condition, and population density. We collected 632 ptarmigan in northeast Iceland in early October from 2006 to 2012; 630 (99.7%) were infected with at least one parasite species, 616 (98%) with ectoparasites, and 536 (85%) with endoparasites. We analysed indices for the combined parasite community (16 species) and known pathogenic parasites, two coccidian protozoans Eimeria muta and Eimeria rjupa, two nematodes Capillaria caudinflata and Trichostrongylus tenuis, one chewing louse Amyrsidea lagopi, and one skin mite Metamicrolichus islandicus. Juveniles overall had more ectoparasites than adults, but endoparasite levels were similar in both groups. Ptarmigan population density was associated with endoparasites, and in particular prevalence of the coccidian parasite Eimeria muta. Annual aggregation level of this eimerid fluctuated inversely with prevalence, with lows at prevalence peak and vice versa. Both prevalence and aggregation of E. muta tracked ptarmigan population density with a 1.5 year time lag. The time lag could be explained by the host specificity of this eimerid, host density dependent shedding of oocysts, and their persistence in the environment from one year to the next. Ptarmigan body condition was negatively associated with E. muta prevalence, an indication of their pathogenicity, and this eimerid was also positively associated with ptarmigan mortality and marginally inversely with fecundity. There were also significant associations between fecundity and chewing louse Amyrsidea lagopi prevalence (negative), excess juvenile mortality and nematode Capillaria caudinflata prevalence (positive), and adult mortality and skin mite Metamicrolichus islandicus prevalence (negative). Though this study is correlational, it provides strong evidence that E. muta through time-lag in prevalence with respect to host population size and by showing significant relations with host body condition, mortality, and fecundity could destabilize ptarmigan population dynamics in Iceland.
... However, such high and stable nest temperatures during incubation, maintained by high incubation constancy, also favour nest-living ectoparasites (fleas, lice and ticks), as abundances of ectoparasites in the nests have been observed to increase in a favourable thermal microclimate (Sinclair & Chown 2006). Accumulating evidence shows that ectoparasites have substantial negative effects on incubating birds due to loss of blood and increased probabilities of infections (Möller 1993, Oppliger et al. 1994, Bush et al. 2001, Lesna et al. 2009, Clayton et al. 2010, Mainwaring et al. 2014, Stenkewitz et al. 2015. ...
Capsule: The occurrence of high numbers of ectoparasites in nests of Common Eiders may be related to nest densities and nesting behaviour.Aims: To estimate abundances of ectoparasites and occurrence of blood-covered eggs, and relate those to nest bowl ages, nest bottom material and the incubation stages of eggs, in nests at two different Common Eider colonies.Methods: Nests were collected at Hvallátur and Rif, two sites at Breiðafjörður, West Iceland, in June and July 2012. The nest bottom material was classified to vegetation species and invertebrates were identified to species when possible.Results: The flea Ceratophyllus garei was the dominant ectoparasite at both sites, with median abundances higher at Hvallátur than at Rif in June. In July, the mean abundance of fleas was higher than observed in June at Rif. There were positive relationships between the flea abundances and the incubation stages of the nests, the blood cover of the eggs and the type of nesting material. No relationship was observed between the age of nesting bowls and adult flea abundances.Conclusion: Disadvantages of large parasite loads on the later nesters (second clutch in each nest) at Rif may be compensated by shared nest attendance and the concurrent added time for preening for females while other females attend their nests.
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Tilraunastöð Háskóla Íslands í meinafræði að Keldum er eini vettvangurinn í landinu þar sem rannsóknir fara fram á dýrasjúkdómum á mörgum fræðasviðum. Tilraunastöðin starfar fyrst og fremst sem rannsóknastofa á háskólastigi. Rannsakaðir eru sjúkdómar í flestum spendýrategundum Íslands og allmörgum fugla- og fisktegundum. Tilgangur rannsóknanna er að efla skilning á eðli sjúkdóma og skapa nýja þekkingu. Heilbrigð dýr eru forsenda arðvænlegs landbúnaðar og fiskeldis. Einnig er mikilvægi heilbrigðra dýra sem bera ekki sjúkdóma í menn hvati að hagnýtingu rannsóknanna. Mikilvægt er að stofnunin geti brugðist sem skjótast við nýjum og aðkallandi vandamálum á sviði sjúkdómagreininga. Tilraunastöðin tengist Læknadeild Háskóla Íslands og hefur sérstaka stjórn og sjálfstæðan fjárhag. Starfseminni er skipt í þrjár fagdeildir; 1) veiru- og sameindalíffræðideild, 2) bakteríu- og sníkjudýradeild og 3) rannsóknadeild fisksjúkdóma.
The evolution of parasite virulence has been hypothesized to be related to the mode of parasite transmission; horizontally transmitted parasites can afford to damage their hosts more than vertically transmitted parasites because increased virulence does not reduce the probability of transmission to new hosts. This relationship between mode of transmission and virulence would particularly select for improved immune defense in hosts that are subject to horizontally transmitted parasites. Among avian hosts, hole nesters and colonial nesters frequently reuse nest sites because of nest-site limitation, and this results in an increased frequency of horizontal transmission. Comparison of the size of two organs involved in the immune defense between pairs of bird species being either hole or open nesters, or colonially or solitarily nesting birds, respectively, revealed that the size of the bursa of Fabricius and the spleen were consistently larger in hole nesters than in open nesters, and similarly in colonially breeding bird species than in solitarily breeding species. These results support the hypothesis that mode of parasite transmission affects the evolution of immune defence in hosts.
All organisms have evolved defence mechanisms for protection against invasion and establishment by micro-organisms and by metazoan parasites. Although ideally we should include the viruses and bacteria in our current discussion, space precludes such a full consideration. Before discussing immunity to parasites, it will be necessary to outline, in the briefest manner, the components of the defence systems—primarily of mammals.
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.
Literature reviewing the avian spleen, particularly that of psittacines, is scarce. The anatomy, physiology, and response to disease of the avian spleen are significantly different from those of the mammalian spleen. However, there are several methods to assess splenic health, and results of such testing can aid in evaluating systemic disease as well as specific diseases of the spleen. This article briefly discusses the anatomy and function of the avian spleen and describes methods used to assess splenic health. A companion article will discuss diseases of the avian spleen.