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Veterinary Parasitology 195 (2013) 142– 149

Contents lists available at SciVerse ScienceDirect

Veterinary Parasitology

jou rn al h om epa ge: www.elsev ier .com/ locate /vetpar

xodes ricinus infestation in free-ranging cervids in Norway—Atudy based upon ear examinations of hunted animals

jell Handelanda,∗, Lars Qvillera,b, Turid Vikørena, Hildegunn Viljugreina,tle Lillehauga, Rebecca K. Davidsona

Norwegian Veterinary Institute, Pb. 750 Sentrum, 0105 Oslo, NorwayCentre for Ecology and Evolutionary Synthesis (CEES), Department of Biology, University of Oslo, P.O. Box 1066 Blindern, Oslo, Norway

a r t i c l e i n f o

rticle history:eceived 21 December 2012eceived in revised form 5 February 2013ccepted 14 February 2013

eywords:xodes ricinusdultsymphsarvaeo-feedingctoparasiteservidsildlife

oonosisorway

a b s t r a c t

Prevalence, abundance and instar composition of Ixodes ricinus as found on one ear col-lected from 1019 moose (Alces alces), red deer (Cervus elaphus) and roe deer (Capreoluscapreolus), shot during hunting (August–December) 2001–2003, are reported. The animalsoriginated from 15 coastal municipalities (CM), seven municipalities bordering to coastalmunicipalities (BCM) and four inland municipalities (IM), in Norway, between latitudes58–66◦ N. I. ricinus occurred endemically in all CM and BCM up to 63◦30′ N, whereas it wasnon-endemic further north and in the IM. This geographical distribution of the tick alongthe coast of southern Norway was largely in accordance with that reported as far back as the1940s. Our results therefore did not indicate any large scale northwards expansion of I. rici-nus in Norway during the 60 year-period between the two studies. However, the prevalenceof infestation and tick abundance were significantly higher in CM as compared to BCM. Theprevalence and abundance by month were highest during August and September, graduallydecreasing towards December. The considerable prevalence of ticks in November, as wellas findings in December, would seem to indicate a prolonged tick season as compared withthe studies carried out 60 years ago.

A total of 8920 ticks were isolated from 439 of the 603 animals examined in endemicmunicipalities, and the maximum number of ticks found on one single ear was 204. Attachedadult ticks were primarily found among the long hairs at base of the ear, whereas nymphsand larvae were seen all over the outer surface of the pinna, for larvae especially at theedge and tip of the ear. Nymphs were the dominant instar, constituting 74% of the totaltick count. The proportion of larvae and adult ticks was 13% and 12%. A significantlyhigher proportion of adult ticks and lower proportion of immature stages were foundin moose, as compared to red deer and roe deer. The same apparently size-associatedpreference of adult ticks was also found for adult animals (all species) as compared tocalves.

Other grossly detected ectoparasites included the lice Solenopotes burmeisteri in red deer

and Damalinia meyeri in roe deer, and the deer ked fly, Lipoptena cervi, in moose and roedeer. This is believed to be the first systematic study on the instar composition by I. ricinusinfestation in free-ranging cervids. The examination of ears from hunted cervids should

ration

be recognized as a abundance of this tick in n

∗ Corresponding author. Tel.: +47 23216350; fax: +47 23216095.E-mail address: kjell.handeland@vetinst.no (K. Handeland).

304-4017/$ – see front matter © 2013 Elsevier B.V. All rights reserved.ttp://dx.doi.org/10.1016/j.vetpar.2013.02.012

al way of obtaining data on the geographical distribution and

ature.

© 2013 Elsevier B.V. All rights reserved.

ry Paras

K. Handeland et al. / Veterina

1. Introduction

Ticks (Acari, Ixodidae) are important ectoparasites andvectors of disease both in man and other vertebratesand 8 endemic species have been recognized in Norway(Mehl, 1983). The most abundant species, Ixodes ricinus,has long been found along the coast of southern Norway(Tambs-Lyche, 1943). Here, it is a well-known vector ofvarious diseases recognized both in humans (Bjørnstad andMossige, 1955; Skarpaas et al., 2002) and other mammals(Tambs-Lyche, 1943; Jenkins et al., 2001; Stuen, 2003). I.ricinus is not normally found in typical inland regions, ornorthernmost parts, of Norway, reflecting climatic limita-tions for its free-living stages (Tambs-Lyche, 1943; Mehl,1983). However, climate change is likely to expand the liv-ing area and abundance of I. ricinus in northern Europe(Gray et al., 2009). Studies in Sweden have indicated anincreased geographical distribution and density of this ticksince the climate started to noticeably change in the 1980s(Tälleklint and Jaenson, 1998; Lindgren et al., 2000), andin Norway, indications of a spread into regions at higherlatitudes and altitudes were recently reported (Jore et al.,2011).

In Norway, there are large populations of free-rangingred deer (Cervus elaphus), roe deer (Capreolus capreolus),and moose (European elk, Alces alces), acting as hosts forI. ricinus. During the past few decades there has beenan enormous growth within these populations (Solberget al., 2009; Statistics Norway, 1975–2011). Climate changealong with these higher reported densities of suitable hostsmay result in greater local tick abundance and a wider tickdistribution in Norway.

I. ricinus is a three-host tick and the life cycle usuallyrequires three years (Randolph, 2004; Sonenshine, 2005).The tick feeds for only a few days each year (transient par-asite); as a larva in the first year, a nymph in the second,and as an adult in the third. Predilection sites reportedin domestic ruminants are the ears, head, neck, axilla,flank, udder and inguinal region (Milne, 1947; Evans, 1951;L’Hostis et al., 1994). The host preference is regarded tobe small mammals (rodents) for larvae, somewhat largeranimals like birds, rabbits and squirrels for nymphs, andlarger mammals like sheep, cattle and cervids for adultticks (Milne, 1949; Taylor et al., 2007). Detailed studiesof Ixodes infestation and instar composition in Europeancervids are lacking, except for roe deer (Carpi et al., 2008;Vor et al., 2010; Kiffner et al., 2011). None of the pub-lished roe deer studies provide specific information abouttick load on the ears of the examined animals. Mattheeet al. (1997), on the other hand, carried out a thoroughstudy of ixodid tick infestation in impala (Aepyceros melam-pus). They found that one third of the total body tickload was localized on the ears of the animals. Similarly ahigh tick load may also be expected on ears from cervids,which serve as effective antenna for questing ticks that arepresent in the greatly diverse vegetation eaten by thesespecies.

The present study reports the prevalence, abundanceand instar composition of I. ricinus, as found on ears col-lected from red deer, roe deer and moose shot in differentregions of Norway during the hunting seasons 2001–2003.

itology 195 (2013) 142– 149 143

2. Materials and methods

2.1. Cervids and ear examinations

The Norwegian populations of red deer are primarilyfound in West and Central Norway, roe deer in East andCentral Norway, whereas moose are common in all partsof the country except for West Norway (Reimers et al.,1990; Solberg et al., 2009). The annual hunting bag isapproximately 100,000 animals, almost equally distributedbetween the three species (Statistics Norway, 1975–2011).The licensed hunting periods are as follows: adult maleroe deer from August 16 to December 23 and other agecategories of roe deer from September 25 to December23. Red deer hunting takes place from September 10 toNovember 15, whereas moose are hunted from September25 to October 31.

In the present study one ear was collected from eachof 440 moose, 263 red deer and 316 roe deer, shot duringlicensed hunting seasons in 2001–2003. The animals orig-inated from 26 different municipalities located betweenlatitudes 58◦ and 66◦ N of East (Nos. 1–17), West (18–21),Central (22–25) and North Norway (26) (Fig. 1 and Table 1).Fifteen of the municipalities have a coastal line and aredefined as coastal municipalities (CM), a further sevenare inland municipalities which share a border with oneor more coastal municipalities, hereafter called borderingcoastal municipalities (BCM), whereas the remaining fourare true inland municipalities (IM) without any proxim-ity to the coast. In the vast majority of municipalities onlyone species of cervid was sampled with the exception of 12Tvedestrand and 22 Hitra where two species were sampled.Different cervid species were sampled during differentyears: red deer were sampled during the 2001 huntingseason, roe deer were sampled in 2002, and moose weresampled, with the exception of 12 Tvedestrand (2002), in2003.

The ear was cut at its base, wrapped and sealed in aplastic bag and sent in by the hunter as soon as possibleafter hunting. The submission was accompanied by a stan-dardized form that gave information on the sex, age (calf,adult), location, and date of killing. Upon arrival at the labo-ratory, the ear and the inside of the plastic bag were studiedunder good light conditions in order to identify parasites.The complete pinna was carefully inspected and system-atically palpated throughout its length, starting in the hairrim at the base of the ear and working towards the tip.All parasites found were placed in 70% alcohol, and all tickswere subsequently separated into instar categories (larvae,nymphs, adults) and counted. A minimum of 10 individ-ual ticks from each instar stage and ear were speciated,where possible, according to descriptions given by Arthur(1963).

2.2. Statistical methods

The statistical analyses were performed using the R sta-

tistical software version 2.15 (R Development Core Team,2011), with extension packages: lme4, mlogit and glm-mADMB. A significance level of 5% was selected (p ≤ 0.05)for the purpose of statistical analyses.

144 K. Handeland et al. / Veterinary Parasitology 195 (2013) 142– 149

Fig. 1. Map of Norway up to southern North Norway showing sampling municipalities of the ears examined from red deer, moose and roe deer shot duringthe licensed hunting 2001–2003: (1) Etnedal, (2) Ringsaker, (3) Grue, (4) Trøgstad, (5) Ås, (6) Vestby, (7) Holmestrand, (8) Horten, (9) Lardal, (10) Bamble,( , (16) MaH ities foun

ma

gr(bas

tm

11) Risør, (12) Tvedestrand, (13) Åmli, (14) Kristiansand, (15) Songdalenitra, (23) Levanger, (24) Åfjord, (25) Namsos and (26) Vefsn. Municipalon-endemic municipalities in green.

Three types of model were developed, using backwardodel selection, to investigate tick prevalence data, tick

bundance data and tick instar composition.Tick prevalence data (0 or 1) were analysed with a

eneralized linear mixed model (GLMM) using logisticegression. Explanatory variables included coastal regionCM versus BCM), month and squared month. Month num-ers were centred on October. Municipality was includeds a random intercept term, in order to account for any

patial dependency of the data.

The tick abundance data was investigated using a nega-ive binomial mixed model. Explanatory variables in the

ain model included coastal region (CM versus BCM),

rnardal, (17) Lyngdal, (18) Gaular, (19) Eid, (20) Hareid, (21) Molde, (22)nd to be endemically infested with Ixodes ricinus are marked in yellow,

month and squared month (month number centred onOctober). The main model was then checked for consis-tency by including the variables host species and age (calfversus adult).

A multinomial logistic regression model was used toinvestigate tick instar proportions. Larvae, nymph andadult ticks were modelled as a function of host speciesand age (calf versus adult). We only used October data tocompare tick instar composition between the three host

species as this was the only month with moose data. Wethen carried out a similar analysis for roe deer and red deeronly as the hunting season is longer for these host species.Tick instar composition (larvae, nymph and adult) was

K. Handeland et al. / Veterinary Parasitology 195 (2013) 142– 149 145

Table 1Prevalences of Ixodes ricinus infestation, and mean tick abundance in tick positive animals, as found by examination of one ear from 1019 red deer, mooseand roe deer hunted in 26 different municipalities in Norway, 2001–2003.

Municipality Type of municipality Species No. examined No. tick-positive % positive Mean tick abundance

1. Etnedal IM Moose 51 0 0 02. Ringsaker IM Roe deer 26 1 4 13. Grue IM Moose 88 0 0 04. Trøgstad IM Roe deer 28 1 4 15. Ås BCM Roe deer 7 6 86 46. Vestby CM Roe deer 31 21 68 97. Holmestrand CM Roe deer 7 6 86 88. Horten CM Roe deer 27 20 74 379. Lardal BCM Moose 58 27 47 310. Bamble CM Moose 49 39 80 711. Risør CM Roe deer 15 13 87 3612. Tvedestrand CM Moose 39 39 100 18

Roe deer 11 10 91 3913. Åmli BCM Roe deer 9 9 100 514. Kristiansand CM Roe deer 26 24 92 4615. Songdalen BCM Roe deer 6 6 100 2916. Marnardal BCM Moose 36 14 39 317. Lyngdal CM Roe deer 9 7 78 2418. Gaular BCM Red deer 51 15 29 1419. Eid BCM Red deer 55 36 66 1320. Hareid CM Red deer 65 62 95 3521. Molde CM Roe deer 6 4 67 7122. Hitra CM Red deer 53 46 87 24

Roe deer 43 31 72 1023. Levanger CM Roe deer 38 2 5 124. Åfjord CM Moose 63 1 2 3

6

6

inland m

were significantly higher in CM as compared to the BCM.Both prevalence and tick abundance (Fig. 3) declined fromAugust and September towards December.

25. Namsos CM Red deer 626. Vefsn CM Moose 5

CM = coastal municipality; BCM = bordering to coastal municipality; IM =

modelled as a function of month, squared month (monthnumber centred on October), host species (roe deer versusred deer) and age (calf versus adult). December data wereexcluded from the tick instar analyses because of limiteddata size. Two way interactions, between host species, ageand month, were investigated to check for consistency.

3. Results

Live larvae, nymphs and adult stages of ticks were foundfree on the inside of the plastic bag, as well as free orattached (blood-filled) throughout the outer surface of theear. The ticks were only occasionally seen on the hairlessskin of the inner ear surface. Attached adults were primar-ily found among the long hairs at base of the ear (Fig. 2),whereas nymphs and larvae were seen all over the surfaceof the pinna, for larvae especially at the edge and tip of theear. In total, 8927 ticks were collected, and the maximumnumber of ticks found on one single ear of moose, red deerand roe deer was 74, 202 and 204, respectively. All of the4740 ticks collected that were speciated were determinedto be I. ricinus. The other parasites occasionally found on theexternal ear surface included the lice Solenopotes burmeis-teri in red deer and Damalinia (syn. Cervicola) meyeri in roedeer. The deer ked fly, Lipoptena cervi, was seen in mooseand roe deer from municipalities in the south-eastern partof East Norway (Fig. 1; Nos. 3–6 and 8), but not elsewhere.

Eight of the municipalities (1–4, 23–26) examined werefound to be non-endemic for ticks, with only occasionaltick positive animals and low mean tick abundance ofinfested individuals (Table 1 and Fig. 1). The remaining 18

0 0 00 0 0

unicipality.

municipalities (5–22) were endemically infested, and tick-positive roe deer occurred as late as December in half themunicipalities with this species. The prevalence in thesemunicipalities varied between 39% and 100%, and the tickabundance between 3 and 71. A total of 8920 ticks wereisolated from cervids from endemic municipalities: 6638(74%) were nymphs, 1183 (13%) larvae, and 1099 (12%)adult ticks. The results on an animal species level, aresummarized in Table 2. Tick abundance and prevalence

Fig. 2. An ear from a red deer with attached (blood-filled) adults andnymphs of Ixodes ricinus. Adult ticks are seen at the base of the ear (right)and nymphs at the adjacent part of the pinna (left).

146 K. Handeland et al. / Veterinary Parasitology 195 (2013) 142– 149

Table 2Prevalence of Ixodes ricinus infestation, mean tick abundance, as well as total number of ticks and their distribution on instar categories, by animal species, asfound by examination of one ear from 603 red deer, moose and roe deer hunted in 18 tick-endemic municipalities in coastal southern Norway, 2001–2003.

Species No. of animals No. of tick-positive (%) Mean tick abundance Total no. of ticks Larvae (%) Nymphs (%) Adults (%)

Red deer 197 159 (81) 25 3906 416 (11) 3094 (79) 396 (10)Moose 182 123 (68) 9 1106 146 (13) 664 (60) 296 (27)Roe deer 224 157 (70) 25 3908 621 (16) 2880 (74) 407 (10)

Table 3Pairwise comparisons of the number of larva relative to adults, nymphs relative to adults and larvae relative to nymphs, in hunted red deer, moose and roedeer in Norway 2001–2003. >, < and NS means larger than, smaller than and not significant, respectively.

Larvae/adults Nymphs/adults Larvae/nymphs

Moose versus red deer NS Moose < red deer Moose > red deerMoose versus roe deer Moose < roe deer Moose < roe deer NS

htts

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l

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Red deer versus roe deer Red deer < roe deerCalf versus adultsa Calf > adultsa

a Not significant for moose.

The modelling of instar composition in relation to theost size (species and age) found a significant increase inhe proportion of adult ticks with increasing body size ofhe host (Table 3). The reverse was found for the nymphaltage.

We found a significant interaction between species andonth when investigating the instar composition on all

hree host species by month. In order to simplify interpre-ation, instar composition was modelled by month for redeer and roe deer (Fig. 4). In roe deer, the proportions of lar-ae and adults were highest and the proportion of nymphsowest, in August and September. The red deer showed anpposite trend, with the lowest counts of larvae and adultsnd the highest counts of nymphs in September.

. Discussion

This is believed to be the first study reporting preva-ence, abundance and instar composition of I. ricinus

0

10

20

30

40

50

60

Tic

k ab

unda

nce

Aug Sept Oct Nov Dec

CMBCM

ig. 3. Monthly variation in Ixodes ricinus abundance as found on ears col-ected from hunted red deer, moose and roe deer in Norway, 2001–2003.ines show predicted tick abundance (with 95% confidence envelopes)s a function of month in coastal (CM) and bordering to coastal (BCM)unicipalities.

Red deer < roe deer NSCalf > adultsa NS

infestation in free-ranging moose and red deer popula-tions. High tick loads were found on the ears of all threespecies examined, with the highest tick counts recordedon a single ear from roe deer and red deer exceeding 200ticks. The examination of ears from hunted cervids shouldbe recognized as a rational way of obtaining data, both oninfestation levels in these species, as well as on the geo-graphical distribution and abundance of this tick in nature.Especially the roe deer, normally living in stationary fam-ily groups (Reimers et al., 1990), should be consideredto reflect the local tick abundance. This high concentra-tion of ticks on the ears of cervids also makes the ears asuitable site for transmission of pathogens between ticksthrough co-feeding, which is regarded as an importantmechanism in the epidemiology of tick-borne pathogenssuch as the tick-borne encephalitis virus (Labuda et al.,1993) and Borrelia burgdorferi sensu lato (Gern and Rais,1996).

This study found that cervids are endemically infestedand important maintenance hosts for I. ricinus along thecoast of East and West Norway up to Hitra (63◦30′ N), witha falling gradient from the coast towards inland regions.Infestation was non-endemic in typical inland regions ofthe country and further north and the few low-grade infes-tations detected here presumably reflected the presenceof smaller discontinuous tick foci. The geographical andseemingly continuous distribution of I. ricinus along thecoast of southern Norway up to Hitra was largely in accor-dance with findings as far back as the 1940s (Tambs-Lyche,1943). Our results therefore did not indicate any continu-ous large scale northward expansion of I. ricinus in Norwayduring the 60 year time-period between the two stud-ies. This does not mean that the tick is absent furthernorth, but may exist where local climatic conditions arefavourable. This tick has, for example, long been recognizedin the municipality of Brønnøysund (65◦30′ N) (Tambs-Lyche, 1943), which was not included in the present study.Furthermore, in a recent study, based on multisource analy-

sis of tick-sighting reports and surveillance data on humanand animal tick-borne diseases, Jore et al. (2011) foundindications of tick presence in coastal municipalities as farnorth as 69◦ N.

K. Handeland et al. / Veterinary Parasitology 195 (2013) 142– 149 147

0.0

0.5

1.0

Aug Sept Oct Nov

Adult roe deer

0.0

0.5

1.0

Sept Oct Nov

Adult red deer

0.0

0.5

1.0

Sept Oct Nov

Roe deer calves

0.0

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Sept Oct Nov

Red deer calves

Pre

dict

ed p

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ies

Adult

Nymph

Larvae

om hunge and

Fig. 4. Proportion of instar stages by month as found on ears collected frtick instar data were modelled (multinomial regression) as a function of a

Gray et al. (1992) and Gilbert et al. (2012) described astrong positive relationship between densities of deer andabundance of I. ricinus and the tick counts found in cervidsin the present study may very well reflect local increases intick abundance in response to the great expansion in cervidpopulations seen in Norway during the last few decades(Solberg et al., 2009; Statistics Norway, 1975–2011). Wefound that all three cervid species are important hostsfor all three instar categories of I. ricinus, with nymphs asthe dominant stage. Adult ticks were preferentially seenin moose, and adult animals, whilst the immature stagesexhibited a higher preference for the two smaller species,and calves. A positive correlation between adult tick bur-dens and body mass was also demonstrated in a study inroe deer in Germany (Vor et al., 2010). These findings couldpartly reflect larger sized animals feeding higher up in thevegetation, where adult ticks prefer to quest (Randolph,2004; Sonenshine, 2005). Also the seemingly lower total

tick abundance found in moose, as compared to the twoother species, could be related to this higher up feedingbehaviour of the moose (browser) where immature tickstages are scarce.

ted red deer and roe deer in Norway, 2001–2003, when for each species,month.

It remains however an open question as to whether theinstar composition found on ears of cervids in the presentstudy is representative for the rest of the body surface. Forexample, Ogden et al. (1998) reported a great interstadialvariation in the attachment sites of I. ricinus on sheep, withlarvae preferentially being located on the distal limbs androstral areas of the head, adults on the proximal parts ofthe limbs and around the neck and head, and nymphs inlocations between the larvae and adults. Interestingly, asimilar spatial aggregation of the different instars, as foundon the body level for sheep, seemed to be valid for ears ofcervids, with larvae being present at the tip and edges of thepinna, adults at the base of the ear, and nymphs in the areabetween these two sites. In roe deer in Germany, larvaewere mostly found on the head and forelegs, nymphs onthe head, and adult ticks on the neck (Kiffner et al., 2011).Carpi et al. (2008) examined the lower part of the forelegsof roe deer in Italy and reported high numbers of ticks of

which almost 90% were larvae.

In Norway, like the rest of northern Europe, there aretwo main activity periods for questing I. ricinus, one inthe spring and early summer (March–June) and another

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48 K. Handeland et al. / Veterina

n late summer and autumn (August–October) (Tambs-yche, 1943; Gray, 1991). Ticks are usually more abundanthe first period, and if this period had been included inhe present study, an even higher prevalence and abun-ance of infestation would probably have been found. Vort al. (2010) reported 2.5 times higher mean tick num-ers on German roe deer examined in May, as comparedo September. The present study also found a consider-ble prevalence of infestation in November and even tickositive animals in December, indicating some tick activityotentially throughout the year in endemic coastal areas.his was longer than the tick season previously reported inorway, which documented exceptional cases of tick infes-

ation in November and none in December (Tambs-Lyche,943). This seemingly extended seasonality of tick activityould be a result of longer periods with suitable tempera-ures and moisture for tick activity linked to climate changePerret et al., 2000).

In the present study, we found a peak in tick preva-ence and abundance in August and September, decreasinguring October to December. Proportions of larvae anddults were highest in August for roe deer, while nymphseached their relative maxima in October. This later peak-ng of nymphs as compared to the two other instars is inccordance with observations made in other studies (Gray,991). Red deer, on the other hand, showed a decrease inhe proportion of nymphs and a corresponding increasen the proportion of adults and larvae during the redeer hunting season (September–November). This speciesifference could be attributed to the fact that red deer orig-

nated from the west coast, with a humid maritime climate,hilst roe deer came from eastern regions with a drier andore continental climate.In conclusion, the present study found that red deer,

oe deer and moose in coastal areas of southern Norwayre heavily infested with I. ricinus. Their presence in denseopulations makes cervids important maintenance hostsf the tick in this country. All three host species wereommonly infested with all instars, especially nymphs,ith overall trends of a higher proportion of adults versus

mmature stages in the moose, as compared to red deernd roe deer, and in adult animals (all species) as comparedo calves. The examination of ears from hunted cervidshould be recognized as a rational way of obtaining datan the geographical distribution and abundance of thisick in nature.

cknowledgements

We would like to thank all the hunters who contributedo this study. We also thank Reidar Mehl (Norwegian Insti-ute of Public Health) for his guidance with regard to theick species identification; Tom Andersen (University ofslo) for statistical advice; Attila Tarpai (National Vet-rinary Institute) for designing Fig. 1; and Bjørn GjerdeNorwegian School of Veterinary Science) for taking thehotograph shown in Fig. 2.

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